A Review of Paleozoic and Mesozoic Animal Sounds

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Historical Biology Vol. 20, No. 4, December 2008, 255–287

REVIEW Voices of the past: a review of Paleozoic and Mesozoic animal sounds Phil Senter* Department of Natural Sciences, Fayetteville State University, 1200 Murchison Road, Fayetteville, NC 28301, USA (Received 10 March 2009; ﬁnal version received 6 May 2009)

Here, I present a review and synthesis of fossil and neontological evidence to ﬁnd major trends in the pre-Cenozoic evolution of animal acoustic behaviour. Anatomical, ecological and phylogenetic data support the following scenario. Stridulating insects, including crickets, performed the ﬁrst terrestrial twilight choruses during the Triassic. The twilight chorus was joined by water boatmen in the Lower Jurassic, anurans in the Upper Jurassic, geckoes and birds in the Lower Cretaceous, and cicadas and crocodilians in the Upper Cretaceous. Parallel evolution of defensive stridulation took place multiple times within Malacostraca, Arachnida and Coleoptera. Parallel evolution of defensive and courtship-related sound production took place in Actinopterygii, possibly as early as the Devonian. Defensive vocalisations by tetrapods probably did not appear until their predators acquired tympanic ears in the Permian. Tympanic ears appeared independently in Diadectomorpha, Seymouriamorpha, Parareptilia, Diapsida and derived Synapsida. Crocodilians and birds acquired vocal organs independently, and there is no anatomical evidence for vocal ability in bird-line archosaurs basal to the avian clade Ornithothoraces. Acoustic displays by non-avian dinosaurs were therefore probably non-vocal. Other aspects of the evolution of acoustic behaviour in these and other lineages are also discussed. Keywords: acoustic behaviour; vocalisation; hearing; Crustacea; Insecta; Orthoptera; Coleoptera; Hemiptera; Crocodylia; Aves; Mammalia

Introduction far, most paleobioacoustical research has been concen- The fossil record does not include audio recordings. As a trated on the study of the evolution of hearing in tetrapod result, few researchers lose sleep over such questions as vertebrates (e.g. Reisz 1981; Allin 1986; Wu 1994; Clack whether Triceratops heard crickets chirping in the evening, and Allin 2004; Vater et al. 2004) and the evolution of whether Mesozoic treetops resounded with birdsong or sound production in the insect orders Orthoptera and Hemiptera (e.g. Sweet 1996; Rust et al. 1999; Be´thoux and frogsong, or whether the immense corpses of sauropods Nel 2002; Gorochov and Rasnitsyn 2002). However, many were surrounded by the buzzing of bottle flies. Questions other paleobioacoustical issues can be addressed with such as these seem silly at first but are nevertheless available data from fossil and neontological evidence. For worthwhile to ask for three reasons: (1) inferable acoustic example, the first appearances of fossils of sound- details must be included if the paleontologist is to producing taxa can be used to constrain the times of accomplish one of paleontology’s main goals: the origin of their characteristic sounds. Also, knowledge of reconstruction of the ancient world in as much detail as directional selection on extant animal sounds can be used possible, (2) acoustic signals are of great importance to to infer characteristics of the sounds produced by their Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 many animals, so the reconstruction of the lifestyles of ancestors. In addition, because the functions of animal ancient organisms must take acoustic signals into sounds depend on their reception by the intended consideration, and (3) many studies have addressed recipients, information on the evolution of hearing can whether or not extinct animals could hear (e.g. Reisz be used to constrain the times of origin of certain animal 1981; Wu 1994; Clack and Allin 2004), so it is reasonable sounds. For example, one can reasonably infer that certain to ask what they heard. courtship sounds, territorial sounds and other sounds Bioacoustics, the study of animal sound production directed at conspecifics were absent in taxa that lacked and reception, is a rich field with much to offer the appropriate sensory structures. Similarly, one can also paleontologist for application to the study of sound reasonably infer that certain anti-predator sounds were production and reception in fossil animals. Such absent before the appearance of predators with appropriate application could aptly be called paleobioacoustics. Thus sensory structures. Much information pertinent to the

*Email: [email protected]

ISSN 0891-2963 print/ISSN 1029-2381 online q 2008 Taylor & Francis DOI: 10.1080/08912960903033327 http://www.informaworld.com 256 P. Senter

reconstruction of ancient acoustic behaviour has been published, but before now no attempt has been made to pool available information to illuminate broad trends in such behaviour across large geologic time spans. Here, I present a review of the available literature so as to perform such a synthesis for the Paleozoic and Mesozoic Eras.

Major themes in the evolution of aerial sound production and reception Sound reception Most invertebrates are aquatic, and several lineages have independently evolved sense organs that perceive water displacement (Budelmann 1992a,b; Coffin et al. 2004). However, it is difficult to say whether most possess a true sense of hearing, both because the definition of ‘hearing’ varies among researchers and because in aquatic environments the distinctions between sound, vibration and water flow are blurred (Budelmann 1992b). In any case, among extant invertebrates acoustic communication is unknown outside Arthropoda, and there is no reason to believe that the case was different among extinct invertebrates. Airborne sound reception is typically accomplished with tympanic ears. In such ears airborne sounds cause vibrations in a thin membrane, the tympanum (Figure 1), internal to which is an air-filled chamber; mechanoreceptors that are linked to the tympanum detect its movement in response to sounds (Wever 1978; Yager 1999; Kardong 2006). Among insects, tympanic ears have appeared independently in Cicadidae (cicadas), Corixidae (water boatmen), Tachinidae (tachinid flies), Sarcophagidae (flesh flies), Neuroptera (lacewings), Mantodea (mantises), Cicindelidae (tiger beetles), Scarabaeidae (scarab beetles), and several times within Orthoptera (crickets and grasshoppers) and Lepidoptera (moths and butterflies) (Yager 1999; Flook et al. 2000; Robert and Hoy 2000; Cˇ okl et al. 2006) (Figure 2). Tympanic ears in cicadas, water boatmen and crickets are associated with intraspecific acoustic communication

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 (Bailey 1991; Gerhardt and Huber 2002; Cˇ okl et al. 2006). Those of tachinid and flesh flies are used to find their cricket hosts when the latter stridulate (Yager 1999; Robert and Hoy 2000). The tympanic ears of lepidopterans, lacewings, mantises, beetles and grasshoppers are tuned to frequencies Figure 1. Sound production (A–D) and reception (E–H) produced by echolocating bats (Mammalia: Chiroptera), the devices of extant animals. (A) Left cheliped of male ghost crab sounds of which stimulate evasive behaviours in these (Ocypode quadrata), ventral view, showing sound-producing stridulatory structures. (B) Male cicada (Pomponia intermedia) insects (Bailey 1991; Yager 1999; Flook et al. 2000). Such with wings and operculum (exoskeletal covering of tymbal) ears are an evolutionary response to predation by bats removed to show sound-producing tymbal. (C) Sagittally (Bailey 1991; Flook et al. 2000) and, like bats, were sectioned larynx of late-term fetal pig (Sus scrofa) in medial therefore absent before the Cenozoic. Courtship sounds of view, showing sound-producing laryngeal vocal cord and grasshoppers and lepidopterans are secondary and appeared laryngeal cartilages mentioned in text, with edges of airway outlined with broken line. (D) Female katydid (Siliquofera after the advent of tympanic hearing in those taxa (Yager grandis), showing tibial tympanum for reception of airborne 1999), and were therefore absent before the Cenozoic. sound. (E) Head of toad (Bufo americanus), left dorsolateral In addition to receptors attuned to frequencies used in view, showing tympanum for reception of airborne sound. (F) intraspecific communication, some cricket ears also have a Skull of turtle (Trachemys scripta), showing posterior skull Historical Biology 257

Figure 2. Phylogeny of insect orders, after Grimaldi and Engel (2005) showing distribution of sound production and tympanic ears (Dumortier 1963b; Aiken 1985; Yager 1999; Virant-Doberlet and Cˇ okl 2004; Drosopoulos and Claridge 2006). Large symbols indicate wide taxonomic distribution within an order, and small symbols indicate limited taxonomic distribution. Filled circles and squares indicate occurrence within a family or families with known pre-Cenozoic fossil records. A, expulsion of air through spiracles; B, loud flight buzzing; P, percussion of body parts against substrate; S, stridulation; T, tymbals; t, tympanic ears; W, wing fluttering. Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 small number of acoustic receptors for much higher In tetrapod vertebrates with tympanic ears, a bony frequencies produced by echolocating bats (Imaizumi and connection transmits vibrations from the tympanum to the Pollack 1999) (Figure 3), a secondary innovation that inner ear, where resulting fluid vibrations stimulate presumably appeared after the Cenozoic appearance of bats. mechanoreceptors (Wever 1978; Kardong 2006). This R mechanism appeared independently in Anura (frogs and toads), Diapsida (lizards, crocodilians, birds and kin) embayment and stapes; the embayment houses an air-filled space and Synapsida (mammals and kin) (Clack and Allin 2004), internal to the tympanum, which is attached to the rim of the embayment, and the stapes conducts auditory vibrations from the and apparently also in the extinct tetrapod groups tympanum to the inner ear. (G) Skull of snake (Boidae, Seymouriamorpha (Ivakhnenko 1987), Diadectomorpha undetermined species), showing stapes and loosely attached (Berman et al. 1992) and Parareptilia (Laurin and Reisz quadrate bone; the quadrate acts as a tympanum, and the stapes 1995) (Figure 4). Whether the tympanic ears of turtles (attached to the quadrate via a cartilaginous extension that is not (Testudines) appeared independently depends on whether shown here) conducts auditory vibrations from the quadrate to the inner ear. ac, arytenoid cartilage; cc, cricoid cartilage; e, or not turtles arose from within Diapsida or Parareptilia, an embayment; f, file; q, quadrate; s, scraper; st, stapes; t, issue that is disputed (e.g. Rieppel and deBraga 1996; Lee tympanum; tc, thyroid cartilage; v, vocal cord. 1997a,b). Osteological evidence, reviewed later in this 258 P. Senter

crabs and kin), Arachnida (spiders, scorpions and kin), Orthoptera (crickets and grasshoppers), Hemiptera (true bugs) and Coleoptera (beetles) (e.g. Dumortier 1963b). Unfortunately for paleontology, arthropod fossils are rarely preserved in enough detail to determine whether or not stridulatory structures are present. An exception is the taxon Orthoptera, in which the stridulatory structures are modified wing veins and can easily be discerned on fossil wings (e.g. Be´thoux and Nel 2002). Stridulation can be effective even if the intended recipient lacks an auditory apparatus. Arthropods often detect the stridulation of conspecifics via substrate-borne vibrations (Crowson 1981; Gogala 1985, 2006; Barth 2002). Stridulation by prey upon seizure by a vertebrate or arthropod predator stimulates the predator’s tactile receptors – and auditory receptors, if present – and often stimulates the predator to release the prey (Masters 1979; Crowson 1981). In many cases the predator’s release Figure 3. Frequencies of peak hearing ranges (white and grey bars) and sound production (black bars) in extant animals. Grey of the stridulating prey may be a hardwired response to an bars represent peak hearing ranges in vertebrates lacking honest warning, for stridulating prey items often follow structures that enhance hearing such as tympana or connections stridulation with painful stimuli (e.g. stinging) or emission between gas bladder and inner ear; note that hearing is restricted of noxious chemicals, or are externally tough and therefore to low frequencies in such groups. The black bar for snakes difficult to eat (Masters 1979). represents hissing. HS, hearing specialist. Information sources: Autrum 1963; Dumortier 1963c; Tembrock 1963; Vincent 1963; Many tetrapod vertebrates (Tetrapoda) produce sounds Simmons et al. 1971; Fant 1973; Gans and Wever 1976; by vocalisation, the vibration of mucosal folds called vocal Marcellini 1977; Garrick et al. 1978; Wever 1978, 1985; Robbins cords that extend into the lumen of the respiratory tract et al. 1983; Hill and Smith 1984; Aiken 1985; Fay 1988; Young (Figure 1). Vocal cords occur in Anura (frogs and toads), 1991; Duellman and Trueb 1994; Frankenberg and Werner 1992; Ambystoma þ Dicamptodon (mole salamanders), Mam- Thorbjarnarson and Hernańdez 1993; Michelsen 1998; Imaizumi þ and Pollack 1999; Ladich and Bass 2003; Young 1991. malia (mammals), Gekkonidae Eublepharidae (geckoes), Pituophis melanoleucus (the bull snake), Crocodylia paper, indicates the presence of tympanic ears in all these (crocodilians), and Aves (birds) (Reese 1914; Maslin groups before the Cenozoic, and in most cases before the 1950; Kelemen 1963; Gans and Maderson 1973; King Mesozoic. As with many insect taxa, it is possible that the 1989; Young et al. 1995). Morphology, topology and original function of tympanic hearing in the various phylogenetic distribution indicate that vocal cords arose tetrapod taxa was predator avoidance. The sounds made by independently in each of these groups (Figure 5). In all but the approach of a large animal often stimulate evasive or Aves the vocal cords are in the larynx (Reese 1914; Maslin cryptic behaviour in extant reptiles (Greene 1988), birds 1950; Kelemen 1963; Gans and Maderson 1973; Young and mammals (personal observation). In predatory taxa et al. 1995); in birds they are in a unique organ called the hearing may have originally facilitated prey localisation. syrinx (King 1989). Many extant predatory tetrapods rely heavily on chemical Percussion is the hitting of a body part against a

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 and visual means of prey localisation (Ewer 1973; substrate. Examples include nuptial abdomen tapping by Duellman and Trueb 1994; Pough et al. 1998), but some stoneflies (Plecoptera) and booklice (Psocoptera) and the use hearing to locate prey (Ewer 1973). aquatic head-slap displays of crocodilians (Pearman 1928; Garrick et al. 1978; Thorbjarnarson 1989; Stewart and Sandberg 2006). These are discussed in more detail below. Sound production Some insects produce defensive sounds by forcing air Methods of animal sound production fall into five main through spiracles (Roth and Hartman 1967; Aiken 1985). categories: stridulation, vocalisation, percussion, forced However, sound production by forceful airflow is more airflow and the tymbal mechanism. Stridulation, the rubbing characteristic of the vertebrate taxon Amniota, many together of body parts, is the most common means of sound members of which hiss by forced ventilation. Hissing as a production in arthropods. Usually one of the stridulatory threat device, often directed at potential predators, is parts (the file) is ridged, while the other (the scraper or widespread among extant amniotes, including lizards, plectrum) is not (Figure 1). Stridulation has evolved snakes, turtles, crocodilians, basal birds and basal convergently in several arthropod groups (Figure 2) and is mammals (Greene 1988; Davies 2002; Kear 2005; especially prevalent among groups with highly sclerotised Nowak 2005). It may therefore be a behavioural (hardened) exoskeletons such as Malacostraca (shrimps, symplesiomorphy for Amniota. If that is correct, then the Historical Biology 259

Figure 4. Phylogeny of vertebrates discussed in this paper, showing independent origins of tympanic ears (T). Extant taxa are indicated

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 with common names in parentheses. See text for information sources.

hiss was present by the Pennsylvanian Period (Ruta et al. ribs (e.g. Kinney et al. 1998). In turtles and birds, hissing is 2003), at which time no vertebrate predator had yet not accompanied by bodily expansion because their acquired tympanic ears (Clack and Allin 2004). ribcages do not allow it. However, hissing in the A Pennsylvanian hiss therefore had no value as an earliest turtles and birds already had value as an acoustic acoustic display unless it exhibited the extraordinary display because tympanic ears were present in a variety of intensity necessary to be heard with atympanic ears. tetrapod predators by the time turtles and birds appeared If hissing is a behavioural symplesiomorphy of Amniota, (reviewed below). its sound may therefore have originally been the passive Tymbals, which are unique to Hemiptera (true bugs), result of a visual, inﬂationary display, as is the case with are series of external folds on the ﬁrst abdominal segment. some extant reptiles (Kinney et al. 1998). A hiss can be Tymbals are buckled by internal muscles to produce produced during inspiration (Kinney et al. 1998; Young substrate-borne vibrations (Leston and Pringle 1963; 1998) or expiration (Gans and Maderson 1973; Young Gogala 1984; Claridge 1985). In cicadas (Cicadidae), 1998). Either way, forced inspiration occurs, and this discussed more fully below, tymbals are coupled with air increases apparent body size in an amniote with movable bladders to produce airborne sounds. 260 P. Senter

(Figure 1) that primitively served as a brace between cheek and braincase (Clack 1992). Due to its opportune location the stapes has been coupled with an external tympanum for transmission of airborne sound to the inner ear in several tetrapod lineages independently (Clack and Allin 2004) (Figure 4). Another example of acoustic parallelism in tetrapods is the parallel evolution of sound-producing vocal cords within the larynx (Maslin 1950; Kelemen 1963; Gans and Maderson 1973) (Figure 5). The plesiomorphic presence of laryngeal muscles that can be evolutionarily co-opted for vocal modulation makes the larynx a particularly appropriate organ to modify for vocalisation. The appearance of elytra in Coleoptera (beetles) and the sclerotisation of the beetle exoskeleton have also encouraged repeated parallel evolution of stridulatory structures in Coleoptera, in which many stridulatory structures are modiﬁcations of the elytra-closing mechanism (Dumortier 1963b). Other examples of acoustic parallelism include the repeated independent appearance of trichobothria (sensory hairs that respond to airborne sounds) within Arachnida (spiders and kin) and Hemiptera (true bugs), tibial tympana in Orthoptera (crickets and kin), use of wings for stridulation in Orthoptera and use of chelipeds for stridulation in Malacostraca (shrimp and kin) (Dumortier 1963b; Gwynne 1995; Sweet 1996; Barth 2002; Be´thoux and Nel 2002; Desutter-Grandcolas 2003).

Figure 5. Phylogenetic distribution of vocal cords in the larynx (L) and syrinx (S) of extant jawed vertebrates. Note the large number of intervening taxa without vocal cords, which indicates Caveats multiple independent origins of vocal cords. Sound-producing structures often fossilise poorly or not at all. Because of this the inference that a given animal sound Temporal patterns was present during a given geological period is rarely Across taxa, certain temporal patterns in sound production certain. If a sound producing structure is present in all are nearly universal. Animals tend to be noisiest at dawn, extant members of a given crown clade, then it is most dusk and night, with very little sound production during parsimonious to infer that the structure was present in the the day (Schneider 1967; Marcellini 1977; Garrick et al. common ancestor of the clade. However, conﬁdence in 1978; Welty and Baptista 1988; Thorbjarnarson and such inferences cannot always be absolute, because in

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 Hernańdez 1993; Zelick et al. 1999; McCauley and Cato some cases the prevalence of acoustic parallelism renders 2000; Gerhardt and Huber 2002). A circannual pattern is hypotheses of homology of acoustic structures and also present across taxa, with more sound production behaviour uncertain even among closely related species. during summers than during winters (Garrick et al. 1978; Even when such an inference is correct, it places only a Aiken 1985; Thorbjarnarson and Hernańdez 1993; Morton tentative bound on the time of origin of the structure, 1996; McCauley and Cato 2000; Gerhardt and Huber because the crown clade may have appeared earlier than its 2002). There is no reason to believe that such temporal earliest known fossils and also because it may be patterns were absent before the Cenozoic. impossible to determine whether the structure was present in fossil members of the lineage that are basal to the crown clade. Another compounding factor is the fact that some Parallel evolution taxa with extant members are not defined as crown clades. Certain body plans are more conducive than others to the The earliest members of such taxa therefore do not evolution of certain sound-producing or -receiving organs, necessarily possess the features characteristic of the crown and parallel evolution of such structures is common in taxa clade. For these reasons the paleobioacoustical inferences with appropriate body plans. For example, posterior and presented here must be treated as hypotheses to test, rather internal to the tetrapod cheek is a bone called the stapes than firm conclusions. Nevertheless, available evidence Historical Biology 261

allows enough inferences to be made to make paleobioa- and possibly by action of the calcareous feeding apparatus coustical studies worthwhile. called Aristotle’s lantern (Fish and Mowbray 1970). Sea urchins are known from as early as the Upper Ordovician; their diversity exploded during the Jurassic Period Pre-Cenozoic paleobioacoustics of non-insect (Kier 1987), at which time their frying sounds presumably invertebrates became more prevalent. Incidental sounds Extant barnacles (Arthropoda: Cirripedia) make crackling sounds during feeding as their appendages scrape Extant squid make a popping sound that appears to be due against their calcareous shells (Budelmann 1992a,b). These to fluttering of mantle lips during expulsion of water from sounds are often continuous due to high population density the siphon (Iversen et al. 1963). Although cephalopods are (Dumortier 1963b). Convergent acquisition of calcareous the only invertebrates outside Arthropoda that possess shells, and presumably crackling sounds, by various organs for unambiguous underwater sound reception lineages of barnacles occurred in the Triassic Period and (modified statocysts) (Coffin et al. 2004), there is no continued through the Mesozoic (Foster and Buckeridge evidence that their locomotor sounds are involved in 1987). Paleozoic barnacles lacked calcareous shells (Wills communication. Cephalopods appeared during the Upper 1963; Schram 1975; Collins and Rudkin 1981) and Cambrian and stem-group squid (Teuthidea) during the therefore probably did not produce the crackling sounds. Upper Triassic (Doyle 1993; King 1993). Squid popping The appendages of non-sessile arthropods sometimes sounds may therefore have existed as early as the Upper produce low-amplitude clicking or ticking sounds during Triassic, and such sounds may have been present as early locomotion when the appendages contact the substrate or as the Cambrian if other cephalopods made them. other body parts. Arthropods are known from early in the However, no extant teuthid family has a known pre- Cambrian Period (Briggs et al. 1993), so their incidental Cenozoic fossil record (Doyle 1993), so if popping sounds locomotor sounds may have been present that early. are restricted to crown-group squid such sounds may have been absent from the Mesozoic. Saltwater mussels (Mollusca: Bivalvia: Mytilidae) attach themselves to the substrate with protein secretions Crustaceans (Arthropoda: Crustacea) from the foot called byssal threads. When a mussel uses its Many members of the crustacean taxon Malacostraca foot for locomotion, the stretching and breaking of the (shrimp, lobsters and crabs) stridulate when seized byssal threads make loud snapping sounds (Fish and (Budelmann 1992a). The taxonomically erratic distri- Mowbray 1970). Summation of the snaps produced by the bution of malacostracan stridulatory structures, along with various colony members produces a continuous crackling their great variety and lack of transitional forms, suggests sound (Fish and Mowbray 1970). The family Mytilidae is multiple parallel origins of stridulation within the group known from as early as the Lower Triassic (Skelton and (Dumortier 1963b) (Table 1). While most malacostracans Benton 1993). Members of several other bivalve families stridulate with hard exoskeletal parts, spiny lobsters use byssal threads as anchors, but only in Mytilidae are the (Palinuridae) stridulate by rubbing a soft plectrum at the threads used in locomotion (Ruppert and Barnes 1994), so base of the antenna over a file beneath the eye; the we should not expect that the snapping sounds were mechanism of the resulting rasping sound resembles that present before the appearance of mytilids. of the bow and string of a stringed instrument (Patek Colonies of sea urchins (Echinodermata: Echinoidea) 2001). The oldest known malacostracans are from the Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 make sustained crackling sounds that have been likened to Upper Devonian (Briggs et al. 1993). The bauplan that the sound of something frying (Fish and Mowbray 1970). allowed repeated evolution of stridulation was therefore Individuals contribute to the sound by movement of spines present that early, and it is possible that anti-predator

Table 1. Malacostracan crustacean families that have stridulating members and are known from before the Cenozoic, and their stridulatory organs.

Taxon Earliest record Location of scraper Location of ﬁle Calappidae (box crabs) Lower Cretaceous Cheliped Cephalothorax Diogenidae (left-handed hermit crabs) Upper Cretaceous Left cheliped Right cheliped Lysiosquillidae (mantis shrimp) Upper Cretaceous Uropods Lower surface of telson Palinuridae (spiny lobsters) Lower Jurassic Base of antenna Antennular plate below eye Penaeidae (prawns) Lower Triassic First abdominal segment Posterior Cephalothorax Squillidae (mantis shrimp) Upper Cretaceous Uropods Lower surface of telson Xanthidae (mud crabs) Lower Cretaceous Cheliped Walking legs

References: Dumortier 1963b; Briggs et al. 1993; Patek 2001. 262 P. Senter

stridulation evolved multiple times in Paleozoic and solifuge and amblypygid are from the Pennsylvanian Mesozoic malacostracan lineages. Stridulatory structures (Selden 1993; Dunlop 1994). The earliest terrestrial have been identified on the flanks of members of the scorpions are from the Devonian (Selden and Dunlop Cretaceous palinurid lobster genus Linuparus (Feldmann 1998). Basal spiders are known from as early as the Lower et al. 2007). Devonian, with representatives of extant clades present by A non-stridulatory malacostracan sound is the buzzing the Pennsylvanian (Mesothelae), Middle Triassic (Myga- of clawed lobsters (Nephropidae) when seized, accom- lomorphae) and Middle Jurassic (Araneomorphae) (Pen- plished by vibrating the carapace (Henniger and Watson ney et al. 2003). Stridulation by or directed toward those 2005). The family is known from as early as the Middle taxa may have been present by those times. Jurassic (Briggs et al. 1993). In addition to defensive stridulation, members of several extant spider families stridulate during courtship or interspecific aggression (Uetz and Stratton 1981), and the Arachnids (Arthropoda: Arachnida) same is conceivably true of members of extinct spider Stridulation in response to disturbance is present in a wide families. Some spiders make courtship sounds by means variety of arachnids, including spiders (Araneae), other than stridulation. Giant crab spiders (Sparassidae) scorpions (Scorpiones), whip scorpions (Amblypygi), vibrate their appendages like tuning forks, and crab spiders windscorpions (Solifugae) and harvestmen (Opiliones) (Thomisidae) drum body parts against the substrate (Dumortier 1963a,b; Uetz and Stratton 1981; Cloudsley- (Uetz and Stratton 1981). Both families were present by Thompson and Constantinou 1984). While the sounds the Cretaceous Period (Grimaldi et al. 2002a,b). produced by arachnid stridulation are often of low Trichobothria, sensory hairs sensitive to air move- intensity and cannot be heard further away than a few ments, have evolved convergently in several extant centimetres, in some cases spider and scorpion stridulation arachnid taxa (Sissom 1990; Barth 2002). The trichobo- produces a loud buzz or hiss (Uetz and Stratton 1981; thria of spiders can detect low-frequency sounds of McCormick and Polis 1990). Only six of the many extant 10–950 Hz, with peak sensitivity from 50 to 120 Hz, and arachnid families with known stridulating members spiders use this ability to locate flying flies and other prey (Dumortier 1963b; Uetz and Stratton 1981) have known (Barth 2002). Extant scorpions use trichobothria to detect pre-Cenozoic fossil records, and all six are spider families air currents caused by prey movements (McCormick and (Selden 1993; Penney et al. 2003) (Table 2). However, the Polis 1990), but it is uncertain whether their trichobothria known pre-Cenozoic fossil record of Arachnida is so are used for sound reception. Either way, Paleozoic spotty that many extant lineages probably existed long scorpions lacked trichobothria (Sissom 1990) and there- before their known fossil records reveal (Penney et al. fore did not locate prey by means of airborne sound. 2003). Also, the wide variety of arachnid stridulatory structures (Dumortier 1963b; Uetz and Stratton 1981; Hjelle 1990) indicates that parallel evolution of stridula- Millipedes and centipedes (Arthropoda: Myriapoda) tion is rampant in Arachnida, which in turn suggests high Some myriapods stridulate in response to disturbance, and likelihood that many extinct arachnids also stridulated in in some cases detached appendages make creaking sounds response to disturbance. A patch of spines found on a limb by an unknown mechanism, apparently to distract a fragment of a Middle Devonian arachnid of unknown predator while the myriapod escapes (Dumortier 1963a,b). affinity from New York may be a stridulatory structure Centipedes (Chilopoda) are known from as early as the Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 (Shear et al. 1987). Upper Silurian (Jeram et al. 1990) and millipedes The earliest known arachnids are from the Silurian (Diplopoda) from as early as the Lower Devonian (Jeram et al. 1990). The earliest known harvestman is from (Shear 1997). Defensive stridulation by myriapods, the Devonian (Dunlop et al. 2003), and the earliest known directed at arachnid or centipede predators, may therefore

Table 2. Stridulating spider families that are known from before the Cenozoic, and their known stridulatory organs.

Taxon Earliest record Location of scraper Location of ﬁle Araneidae (orb weavers) Upper Cretaceous Appendage Abdomen Dipluridae (funnel-web tarantulas) Lower Cretaceous Pedipalp Chelicera Linyphiidae (sheet-web weavers) Lower Cretaceous Pedipalp------Chelicera Leg II------Leg I Segestriidae (tube-dwelling spiders) Upper Cretaceous – – Theridiidae (comb-footed spiders) Cretaceous Abdomen Prosoma Uloboridae (hackled orb weavers) Lower Cretaceous Pedipalp Chelicera

References: Uetz and Stratton 1981; Grimaldi et al. 2002a,b; Penney et al. 2003. Historical Biology 263

have existed this early. However, airborne predator- of specialised abdominal parts on the substrate (producing distracting sounds, such as the creaking of detached a squeak) (Stewart and Sandberg 2006). However, none appendages, would have been ineffective against deaf of these families has a pre-Cenozoic fossil record predators and so were probably absent before terrestrial (Sinitshenkova 2002). tetrapods acquired the ability to hear airborne sounds in the Permian Period (see below). The earliest terrestrial animal communities, from the Crickets and kin (Orthoptera) Silurian Period, included centipedes and arachnids Males of several extant orthopteran taxa stridulate during (Jeram et al. 1990), both of which are predatory. courtship by rubbing together specialised parts of the The earliest known millipedes and basal insects (Insecta) wings, producing sounds with species-specific rhythms. appeared shortly thereafter, in the Lower Devonian Such stridulation often stimulates chorusing and aggres- (Jeram et al. 1990; Shear 1997). Anti-predator stridulation sion from nearby males, and the approach of one male too is known in extant members of all four taxa (Dumortier close to another may elicit a different temporal pattern of 1963a,b; Uetz and Stratton 1981) and may therefore have stridulation called a disturbance song (Dumortier 1963a). existed in these early communities. Anti-predator stridula- Stridulatory wing venation patterns are absent in Paleozoic tion is most likely to have evolved first in taxa with orthopterans, the earliest known of which are from the especially tough exoskeletons or in taxa capable of Pennsylvanian (Be´thoux and Nel 2002; Gorochov and producing unpleasant stimuli such as stings, bites, or Rasnitsyn 2002). Stridulatory mechanisms on the wings noxious emissions, so that it functioned as an honest warning were present in the extinct, Upper Triassic orthopteran to predators, as in extant arthropods (Masters 1979). family Mesoedischiidae and in members of Ensifera (crickets) from the Upper Triassic and later (Be´thoux and Nel 2002; Gorochov and Rasnitsyn 2002). The earliest Directions for further research known members of the extant stridulating ensiferan taxa To my knowledge, stridulatory structures have not been Gryllidae (true crickets) and Gryllotalpidae (mole crick- described in fossil arthropods outside Insecta with the ets) are from the Lower Cretaceous (Ross and Jarzem- exception of the Devonian arachnid and the Cretaceous bowski 1993). Stridulation is also characteristic of lobster mentioned above. A search for stridulatory ‘Prophalangopsidae’ (hump-winged and sagebrush crick- structures among fossil malacostracans, trilobites, eur- ets), a taxon that is probably paraphyletic with respect to ypterids and perhaps other pre-Cenozoic arthropods would Tettigoniidae (katydids) (Desutter-Grandcolas 2003). be worthwhile. It would also be informative to compare ‘Prophalangopsids’ are known from as early as the sound-producing structures across Malacostraca and Lower Jurassic, while katydids, grasshoppers (Acridoi- Arachnida to determine whether any such structures are dea), and other extant orthopteran families with stridulat- homologous between families or genera. ing members have no known pre-Cenozoic fossil record (Ross and Jarzembowski 1993; Rust et al. 1999; Gorochov and Rasnitsyn 2002). Pre-Cenozoic insect paleobioacoustics Extant stridulating crickets simultaneously perceive Stoneflies (Plecoptera) both the substrate-borne vibrations (via mechanoreceptors Intraspecific acoustic communication is characteristic of in the legs) and the airborne sounds (via tibial tympana; the extant stonefly clade Arctoperlaria (Stewart and Figure 1) generated by the singing of conspecifics

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 Sandberg 2006). After emergence, arctoperlarian stone- (Ku¨hne et al. 1985). Morphological phylogenetic analyses flies perform male-female vibratory duets at aggregation of extant ensiferans suggest that stridulatory structures and sites while the males search for the females (Stewart and tibial tympana were absent in the common ancestor of Sandberg 2006). The duets consist of vibrations with extant orthopterans and have evolved in parallel a number species-specific rhythms, produced by audible tapping of of times within the ensiferan crown group (Gwynne 1995; the abdomen on the substrate (Stewart and Sandberg Desutter-Grandcolas 2003). However, stridulatory wing 2006). Tapping duets are known in all extant arctoperlar- venation is present in all members of a long phylogenetic ian families and appear to be a behavioural symplesio- series of Upper Triassic crickets that are basal to crown morphy of the clade (Stewart and Sandberg 2006). If this is Orthoptera (Be´thoux and Nel 2002), which indicates that correct then the resulting sounds were present at the time stridulatory behaviour is plesiomorphic for Upper Triassic of origin of the arctoperlarian crown clade, the earliest and later crickets. This suggests that either stridulation was known fossils of which are from the Middle Triassic lost once in the crown clade’s ancestor and then regained (Grimaldi and Engel 2005). multiple times by its descendants, or that it was present in Members of some extant stonefly families augment the crown clade’s ancestor and was lost multiple times the courtship tapping with scratching of the abdomen on within the crown clade. The latter interpretation is the substrate (producing a raspy sound), or rubbing supported by a recent molecular phylogenetic analysis, 264 P. Senter

the results of which differ greatly from those of to disturbance, most likely as an alarm signal (Kirchner morphological phylogenetic analyses (Jost and Shaw et al. 1994). This behaviour is taxonomically widespread 2006). Most of the non-stridulatory extant families are within Isoptera and may therefore be a behavioural fossorial (Gwynne 1995), and there may be a connection symplesiomorphy for the group (Virant-Doberlet and Cˇ okl between the acquisition of such a lifestyle and the loss of 2004). Early termites are known from most continents in stridulatory behaviour in crickets. the Lower Cretaceous, including Laurasian members of Gryllacrididae (locust crickets and leaf-rolling crick- the extant head-tapping family Termopsidae (Grimaldi ets) are non-stridulating crickets without tympana, some of and Engel 2005). which are fossorial. Males and females duet by drumming the tarsus or abdomen on the substrate (Hale and Rentz 2001). This family is known from as early as the Upper Booklice (Psocoptera) Cretaceous (Ross and Jarzembowski 1993). A widespread behaviour among booklice is the tapping of Among extant orthopterans of various lineages, the abdomen on the substrate by females to call males; it females generally prefer male calls that are longer and makes a ticking or creaking sound (Pearman 1928). occur at higher rates (Gerhardt and Huber 2002). The earliest known booklice are from the Upper Jurassic; If selective pressure for these traits has existed long fossils from as early as the Lower Permian have been enough, then within each orthopteran lineage male calls attributed to Psocoptera but more likely belong to some were originally of shorter duration and occurred at lower related taxon (Grimaldi and Engel 2005). Extant psocop- rates than those of their extant descendants. teran families with tapping species and known pre-Cenozoic Rust et al. (1999) used comparison with extant fossil records include Psocidae (Upper Jurassic) and orthopterans to calculate the dominant frequency of the Trogiidae (Upper Cretaceous) (Rasnitsyn 2002). stridulatory sounds produced by the wings of a Cenozoic fossil katydid. The same may be possible with Mesozoic orthopterans but has not yet been attempted. Stridulatory wing structures are also present in members True bugs (Hemiptera) of the extinct, Middle and Upper Triassic taxon Titanoptera Extant hemipterans comprise ﬁve major clades: Sternor- (¼Mesotitanida). This taxon is closely related to Orthoptera rhyncha (aphids, scale insects and kin), Fulguromorpha and consists of large (wingspans up to 40 cm) insects from (planthoppers), Coleorrhyncha (peloridiid bugs), Prosor- Eurasia and Australia (Gorochov and Rasnitsyn 2002; rhyncha (water bugs, assassin bugs, stink bugs and kin) Grimaldi and Engel 2005). and Clypeomorpha (cicadas, leafhoppers, froghoppers and kin). Members of the latter four clades possess tymbals, which are buckled by internal muscles in species-speciﬁc Roaches (Blattaria) rhythms to produce vibrations called ‘songs’ during Roachlike insects from as early as the Carboniferous courtship and, in some cases, during copulation Period are often placed in Blattaria, but as a group (Leston and Pringle 1963; Gogala 1984; Claridge 1985; Paleozoic ‘roachoids’ are paraphyletic with respect to Sweet 1996). Tymbals are absent in Sternorrhyncha, and Isoptera (termites), Mantodea (mantises), and Blattaria their presence in the other four clades suggests that (true roaches) (Grimaldi and Engel 2005). The earliest the presence of tymbals is a synapomorphy that unites the known members of Blattaria sensu stricto are from the other four clades into a taxon (hereafter called the

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 Lower Cretaceous (Grimaldi and Engel 2005). Many ‘tymbaled superclade’ below) that excludes Sternor- extant roaches make courtship or disturbance sounds by a rhyncha (Sweet 1996). That interpretation of hemipteran variety of means, but most such noisy roaches are phylogeny is supported by molecular systematics members of Blaberidae (Roth and Hartman 1967), which (Campbell et al. 1995; von Dohlen and Moran 1995). is unknown before the Cenozoic (Grimaldi and Engel In most members of the tymbaled superclade the 2005). Members of other roach families are generally tymbals are simple and do not produce airborne sound but silent, although one member of Blattellidae, a family instead cause vibrations in the substrate, usually a plant known from the Lower Cretaceous (Grimaldi and Engel stem (Leston and Pringle 1963; Claridge 1985; Gogala 2005), makes a clicking sound before taking flight, and 1984, 1985, 2006; Sweet 1996). Both sexes sing, lack another blattellid is known to squeak when caught tympana and perceive the songs of conspecifics via (Roth and Hartman 1967). mechanoreceptors in the legs (Leston and Pringle 1963; Claridge 1985; Gogala 1985, 2006; Sweet 1996). This appears to be the plesiomorphic condition for the tymbaled Termites (Isoptera) superclade (Sweet 1996). The earliest known members of Termite soldiers tap their heads on the substrate with a the tymbaled superclade, which is a crown clade, are from rhythm that is recognised by conspecifics, in response the Lower Permian (Shcherbakov and Popov 2002), and Historical Biology 265

the use of tymbals for substrate-borne courtship songs courtship song (Dumortier 1963a). The variety of presumably originated then. stridulatory structures in Prosorrhyncha (Table 3) Within the tymbaled superclade are several taxa in indicates that augmentation of tymbal songs with which courtship is modified such that it produces airborne stridulation arose multiple times in parallel within sounds. The most familiar example is probably the treetop Prosorrhyncha (Leston and Pringle 1963). Trichobothria singing of members of Cicadidae (cicadas), the earliest are present in many prosorrhynchans, fulguromorphs, and known fossils of which are from the Upper Cretaceous coleorrhynchans, but not in clypeomorphs (Sweet 1996). (Turonian) of New Jersey (Grimaldi et al. 2002b). In cicadas They appear to be used as acoustic receptors for low- the females have lost the tymbals, so singing is done only by frequency, low-amplitude, audible song and differences the males, in which the tymbals are elaborate in comparison between the trichobothria of various taxa suggest that they with those of other hemipterans (Leston and Pringle 1963; appeared in parallel multiple times in the tymbaled Claridge 1985). Air sacs internal to the tymbals amplify the superclade (Sweet 1996). songs so that they are audible from several meters away and In the prosorrhynchan taxon Nepomorpha a switch has attract members of both sexes to a congregational area for occurred from the ancestral hemipteran plant-dwelling reproduction (Dumortier 1963a; Claridge 1985). Cicadas habitat to an aquatic one (Shcherbakov and Popov 2002). hear each other’s songs with tympanic ears that are ventral The new habitat required that plant stems be traded for the to the tymbals on the abdomen (Leston and Pringle 1963; watery environment as a medium to carry vibrational Claridge 1985). After attracting a female, a male cicada signals to conspecifics. Accordingly, many nepomorphs changes the rhythm of his song; in some species he also adds stridulate underwater. Among nepomorph families with audible wing-flicking, and in some species the female known pre-Cenozoic fossil records, stridulation is known responds with wing-flicking of her own (Boulard 2006). in Corixidae (water boatmen), Naucoridae (creeping water Some cicada species also have stridulatory structures, the bugs), Nepidae (waterscorpions), and Notonectidae (back- behavioural significance of which is unknown (Boulard swimmers) (Dumortier 1963b). In Corixidae and Noto- 2006). Another enigmatic acoustic behaviour by cicadas is nectidae stridulation by males is known to attract females the drumming of the wings on the substrate in some species, (Dumortier 1963a; Cˇ okl et al. 2006). The variety of especially in those that have lost tymbals altogether nepomorph stridulatory structures (Table 3) suggests that (Boulard 2006). stridulation arose multiple times independently in In many members of Prosorrhyncha, the earliest Nepomorpha. Because evolution of stridulation is rampant known members of which are from the Upper Triassic in Nepomorpha, it may have been present in extinct (Shcherbakov and Popov 2002), tymbal songs are nepomorphs as early as the Upper Triassic, from which augmented by simultaneous, audible stridulation, which time period the earliest nepomorphs are known (Shcher- adds higher frequencies to the songs (Gogala 1984, 1985, bakov and Popov 2002). Non-stridulatory courtship 2006; Sweet 1996). Often, after the female has been sounds (buzzing or chirping) are made by members of attracted by the male’s calling song, he switches to a Belostomatidae (giant water bugs) by expulsion of air

Table 3. Prosorrhynchan families that are known from before the Cenozoic with members that are known to stridulate, and their stridulatory organs.

Taxon Earliest record Location of scraper Location of ﬁle

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 Alydidae (broad-headed bugs) Upper Jurassic Femur Hemelytra Aradidae (ﬂat bugs) Lower Cretaceous Hind femur------Abdomen Hind tibia------Abdomen Coreidae (leaf-footed bugs) Upper Jurassic Pronotum Fore wing Corixidae (water boatmen) Lower Jurassic Fore tarsus------Opposite fore femur Fore femur------Head Cydnidae (burrowing bugs) Lower Jurassic Abdomen Hind wing Lygaeidae (seed bugs) Lower Cretaceous Wing------Abdomen Foreleg------Prosternum Miridae (plant bugs) Upper Jurassic Hind femur Embolium Nabidae (damsel bugs) Upper Jurassic – – Naucoridae (creeping water bugs) Upper Triassic – – Nepidae (waterscorpions) Upper Jurassic Coxa Femur Notonectidae (backswimmers) Upper Triassic Fore femur------Head or fore coxa Tibia------Rostrum Reduviidae (assassin bugs) Lower Cretaceous Rostrum Prosternum Thaumastellidae (no common name) Lower Cretaceous Abdomen Wing

References: Dumortier 1963b; Leston and Pringle 1963; Gogala 1984, 1985, 2006; Aiken 1985; Ross and Jarzembowski 1993; Shcherbakov and Popov 2002. 266 P. Senter

through spiracles (Aiken 1985); belostomatids are known to attract females or repel rival males (Dumortier 1963a; from as early as the Upper Triassic (Ross and Rudinsky and Ryker 1976; Aiken 1985). The broad Jarzembowski 1993). taxonomic span of families with stridulating members and In one nepomorph family, Corixidae (water boatmen) – the wide variety of stridulatory structures shows that known from as early as the Lower Jurassic (Ross and repeated parallel evolution of stridulation is rampant in Jarzembowski 1993) – perception of conspecific stridula- Coleoptera (Table 4). Beetle stridulation may therefore have tion is truly auditory. Water boatmen receive such been present as early as the Lower Permian, from which the vibrations with tympana that are surrounded by air bubbles, earliest beetle fossils are known (Ponomarenko 2002). whereas other nepomorphs use atympanic mechanorecep- Various beetles are also known to make non- tors for reception of water-borne vibrations (Cˇ okl et al. stridulatory sounds. Female members of Anobiidae 2006). Unlike the low-amplitude calls of most nepomorphs, (death-watch beetles), a family known from as early as which are audible to humans only if the bug is close to the the Lower Cretaceous (Ross and Jarzembowski 1993), listener’s ear, the underwater songs of corixids are quite attract males by drumming the head on the substrate loud; resonation by the same air bubbles that enable (Dumortier 1963a). In some members of Buprestidae tympanic hearing in corixids amplifies the songs so that they (metallic wood-boring beetles), a family known from as are audible from beyond the shoreline (Aiken 1985). early as the Middle Jurassic (Ross and Jarzembowski Courtship sounds are not the only sounds made by 1993), members of both sexes drum their abdomens on the hemipterans. Many clypeomorphs cry audibly when substrate and answer each other’s drumming in like caught and during rough treatment (Dumortier 1963a; manner (Crowson 1981). Drumming of body parts against Leston and Pringle 1963; Claridge 1985). Many prosor- the substrate is also known in Cerambycidae (long-horned rhynchans stridulate audibly when caught, including beetles) (Crowson 1981), the earliest known members of members of Cydnidae (burrowing bugs), Lygaeidae which are from the Lower Cretaceous (Ross and (seed bugs) and Reduviidae (assassin bugs) (Dumortier Jarzembowski 1993). Some cerambycids also make 1963a; Leston and Pringle 1963; Gogala 2006). In some purring sounds by vibrating the body within a crevice in reduviid species the female stridulates upon being bark (Dumortier 1963b). Larvae of some members of mounted, deterring the male, if she is unwilling to mate Dytiscidae (predaceous diving beetles), a family known (Lazzari et al. 2006). Members of the prosorrhynchan from as early as the Upper Jurassic (Ponomarenko 2002), family Coreidae (leaf-footed bugs), the earliest known squeak by expelling air through spiracles when disturbed members of which are from the Upper Jurassic (Ross and (Aiken 1985). Larvae of some members of Hydrophilidae Jarzembowski 1993), make sounds by unknown means (water scavenger beetles), a taxon known from as early as (Dumortier 1963b); the biological significance of these the Upper Triassic (Ponomarenko 2002), hiss by an sounds is unclear, and they are probably by-products of unknown mechanism upon disturbance (Aiken 1985). locomotion (Gogala 1985). Among members of Sternor- Members of Elateridae (click beetles), produce a loud rhyncha, some colonies of aphids (Aphididae) make click by snapping a spine on the prosternum into a notch scraping sounds when disturbed (Leston and Pringle on the mesosternum, which suddenly flexes and bounces 1963). These stridulatory sounds are made by rubbing the the beetle and is used to right the beetle when upside-down hind tibiae on rough spots on the abdomen (Dumortier or to make it difficult for predators to hold (Grimaldi and 1963a). The earliest known aphids are from the Lower Engel 2005); the earliest known elaterids are from the Cretaceous (Ross and Jarzembowski 1993). Upper Triassic (Ponomarenko 2002). The wings of

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 Stridulatory structures are known in some fossil members of Scarabaeidae (scarab beetles), a family hemipterans. Members of the stem-hemipteran family known from as early as the Lower Jurassic (Ponomarenko Dysmorphoptilidae possessed a stridulatory apparatus 2002), often buzz loudly during flight. The exoskeletons of with a scraper on the hind knee and the file on the these beetles are particularly tough, so it is possible that underside of the fore wing; the family is known from the the loud scarabaeid flight buzz is an honest warning of Upper Permian to the Upper Jurassic (Shcherbakov and culinary difficulty to potential predators. Popov 2002). A similar stridulatory apparatus is present in Triassic members of the extinct prosorrhynchan family Ipsviciidae (Shcherbakov and Popov 2002). Lacewings and kin (Neuropterida) The supraordinal insect taxon Neuropterida includes the order Raphidioptera (snakeflies) and the sister orders Beetles (Coleoptera) Megaloptera (dobsonflies and alderflies) and Neuroptera Beetles of many extant families produce sounds, often by (lacewings). Courtship in all extant families of Raphi- stridulation (Alexander and Moore 1963; Dumortier dioptera and Megaloptera involves abdominal tremulation, 1963b). Adult and larval beetles often stridulate in response sensed via substrate- (stem- or leaf-) borne vibrations with to disturbance, although some adult males stridulate species-specific rhythms; in Corydalidae (dobsonflies) Historical Biology 267

Table 4. Beetle families that are known from before the Cenozoic in which adults are known to stridulate, and their stridulatory organs, where known.

Taxon Earliest record Location of scraper Location of ﬁle Anobiidae (death-watch beetles) Lower Cretaceous Prosternum Gula Bruchidae (seed beetles) Upper Jurassic – – Buprestidae (metallic wood-boring beetles) Upper Jurassic – – Carabidae (ground beetles) Lower Jurassic Elytra------Abdomen Femur------Elytra Cerambycidae (long-horned beetles) Lower Cretaceous Pronotum------Mesonotum Elytra------Hindfemur Metasternum------Coax Chrysomelidae (leaf beetles) Upper Jurassic Prosternum------Gula Pronotum------Mesonotum Elytra------Abdomen Curculionidae (weevils) Lower Cretaceous Elytra------Abdomen Abdomen------Elytra Dytiscidae (predaceous diving beetles) Upper Jurassic Wing Abdomen Endomychidae (handsome fungus beetles) Upper Cretaceous Pronotum Head Heteroceridae (variegated mud-loving beetles) Lower Cretaceous Femur Abdomen Hydrophilidae (water scavenger beetles) Upper Triassic Elytra Abdomen Lucanidae (stag beetles) Upper Jurassic Elytra Hindfemur Nemonychidae (no common name) Upper Jurassic – – Nitidulidae (sap beetles) Middle Jurassic Pronotum Head Passalidae (bessbugs) Lower Cretaceous Abdomen------Wing Scarabaeidae (scarab beetles) Lower Jurassic Elytra------Abdomen Elytra------Hindfemur Coax------Metasternum Abdomen------Elytra Abdomen------Wing Femur------Elytra Scolytidae (bark beetles and ambrosia beetles) Lower Cretaceous Prosternum------Gula Abdomen------Elytra Silphidae (carrion beetles) Lower Jurassic Elytra Abdomen

References: Dumortier 1963b; Ross and Jarzembowski 1993; Ponomarenko 2002; Wessel 2006.

only the males tremulate, but in Sialidae (alderflies) and neuropterid orders or was present in the common Raphidioptera the sexes perform tremulatory duets neuropterid ancestor, lost in ancestral lacewings, and (Henry 2006). While tremulation does not produce then regained in derived lacewings. If tremulation was airborne sounds, it is often accompanied by audible wing present in the neuropterid ancestor, then it (and possibly fluttering in Raphidioptera or by audible drumming of the the accompanying sounds of drumming and/or wing abdomen on the substrate in Sialidae, and is replaced by fluttering) existed as early as the Permian Period, from audible wing fluttering in some species of Corydalidae which the earliest neuropterid fossils are known

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 (Henry 2006). (Grimaldi and Engel 2005). If tremulation evolved Among lacewings, wing fluttering during courtship is separately in the three orders, then the times of origin of known in Coniopterygidae (dustywings) and Berothidae its separate appearances are less clear. Snakeflies are (beaded lacewings) (Henry 2006), known from as early as known from the Lower Jurassic, but the earliest known the Upper Jurassic and the Lower Cretaceous respectively member of an extant family is from the Tertiary (Grimaldi (Grimaldi and Engel 2005). Tremulation, wing fluttering and Engel 2005). Megalopterans are known from as early and abdominal drumming during courtship are all known as the Upper Triassic, but extant megalopteran families are in Chrysopidae (green lacewings) (Henry 2006), a family unknown before the Middle Jurassic (Grimaldi and Engel known from as early as the Lower Cretaceous (Grimaldi 2005). Estimated times of origin of tremulation and and Engel 2005). accompanying sounds in Raphidioptera and Megaloptera Among lacewings, tremulation is absent in all but three therefore depend on whether tremulation was present in derived families, the relationships between which suggest each order’s ancestor or only in members of extant an independent origin of tremulation in each (Henry 2006). tremulating families. It is plausible that the neuropterid The presence of tremulation in Raphidioptera and bauplan encouraged repeated evolution of tremulation, Megaloptera but not basal Neuroptera makes it unclear just as the beetle bauplan encouraged repeated evolution of whether tremulation appeared independently in the three stridulation. It is therefore possible that these neuropterid 268 P. Senter

behaviours and their accompanying sounds appeared mechanoreceptors in the antennae that detect air movement multiple times before and during the Cenozoic. caused by the vibrations of the wings of conspecifics engaging in thoracic pulsation (Hrncir et al. 2006). Ants (Formicidae) are also members of Aculeata. Wasps, bees and ants (Hymenoptera) The earliest known ants are from the Cretaceous Period Wasps (Hymenoptera) are known from as early as the and include members of four extant subfamilies: Upper Triassic (Grimaldi and Engel 2005). The wasp clade Ponerinae (trap-jaw ants and kin), Dolichoderinae (cone Aculeata, known from as early as the Upper Jurassic, is ants and kin), Formicinae (carpenter ants, wood ants and characterised by modification of the ovipositor into a sting kin), and Myrmicinae (harvester ants, fire ants and kin) (Grimaldi and Engel 2005). Aculeates tend to buzz audibly (Moreau et al. 2006). The earliest known fossil records of in flight, and it is possible that, as with the stridulatory the former two subfamilies are from the Lower sounds of certain other insects, the flight fuzz deters Cretaceous, and those of the latter two are from the potential predators by warning them of the painful Upper Cretaceous (Moreau et al. 2006). Some dolicho- consequences of predatory attempts. derine and formicine ant workers tap their mandibles and Aculeate flight sounds also serve social functions. Some abdomens on the substrate to produce alarm sounds in male braconid wasps (Braconidae) also use their wings to response to nest disturbance (Ho¨lldobler and Wilson make courtship sounds when near females (Sotavalta 1963); 1990). Stridulation is used by ponerine and myrmicine braconids are known from as early as the Lower Cretaceous ants – especially in soil-dwelling species – for group (Ross and Jarzembowski 1993). Members of Vespidae, cohesion, warning of danger, as a call for help by wounded which includes hornets and kin, are known to buzz with or imperiled individuals, and as a signal by females to their wings during flight and during copulation (O’Neill males that copulation is complete (Dumortier 1963a; 2001); vespids are known from as early as the Lower Ho¨lldobler and Wilson 1990). Stridulation occurs by Cretaceous (Ross and Jarzembowski 1993). In some rubbing the last segment of the petiole against the striated members of Sphecidae (mud daubers and kin), a family dorsal edge of the first segment of the gaster in Ponerinae known from as early as the Lower Cretaceous (Ross and and Myrmicinae (Dumortier 1963b); in some myrmicines Jarzembowski 1993), males use buzzing as an acoustic this is coupled with the rubbing of a second, ventral threat when defending the nest against marauders or rival stridulatory apparatus at the joint between the same two males (O’Neill 2001); males of some sphecid species also segments (Dumortier 1963b). In small ant species locate virgin females by the loud buzz made by the females stridulation is inaudible to humans further away than a as they dig themselves out of the ground. The buzzing of few centimetres, but in large members of Ponerinae and bees (Apoidea) cannot be heard by fellow bees during flight, Myrmicinae it can be audible further away (Dumortier but in some bees, once females have alighted, males use the 1963b,c). Ants themselves are deaf to airborne sounds and flight buzz to court them (Sotavalta 1963). The earliest detect conspecific stridulation via substrate-borne known bee is from the Lower Cretaceous (Poinar and vibrations (Ho¨lldobler and Wilson 1990). Danforth 2006). Reports of pre-Cretaceous bee body and Stridulation between edges of abdominal segments is trace fossils exist, but the former have been reidentified as also known in some members of Mutillidae (velvet-ants) indeterminate insects and the latter are more likely beetle (Dumortier 1963b; O’Neill 2001), an aculeate family than bee traces (Engel 2001). known from as early as the Upper Cretaceous (Ross and A variety of sounds are known in extant bees, Jarzembowski 1993). In some species the male makes a

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 particularly those of the closely related tribes Apini honking sound by vibrations of the wings and thorax as he (honeybees and kin), Bombini (bumblebees and kin) and approaches the female, and both members of the pair Meliponini (stingless bees). Sounds that have been alternately stridulate during copulation (O’Neill 2001). described as tooting, quacking, hissing and piping serve various social functions in Apini and Bombini (Hrncir et al. 2006), but neither taxon is known from before the Cenozoic Flies, gnats and mosquitoes (Diptera) (Engel 2001). Stingless bees are known from the Upper Dipterans are known from as early as the Middle Triassic Cretaceous (Engel 2001). Stingless bees share with Apini (Blagoderov et al. 2002). Audible wing vibration by the and Bombini the tendency for foragers to use thoracic male during mounting is widespread in Diptera (Kanmiya pulsation to make sounds that stimulate nestmates to fly out 2006). In addition, many dipterans use flight sounds as a – sometimes after first buzzing in response – and collect means of intraspecific communication. Male mosquitoes food (Hrncir et al. 2006). If thoracic pulsation is a (Culicidae) have a hearing apparatus in the antennae, behavioural symplesiomorphy for stingless bees, honeybees which is used to find the female by her flight hum and to and bumblebees, then it was present at least as early as the keep together in all-male swarms (Sotavalta 1963); the Upper Cretaceous. Bees lack tympanic ears and sense the earliest known mosquitoes are from the Cretaceous sounds of conspecifics via substrate-borne vibrations and via (Grimaldi et al. 2002a,b). Male hover flies (Syrphidae) Historical Biology 269

court females by flying with a high-pitched hum over a or absent and other parts of the inner ear are used for female on a flower (Sotavalta 1963); the earliest known hearing (Popper et al. 1992; Ladich and Popper 2004). hover flies are from the Upper Cretaceous (Blagoderov Cartilaginous fishes are generally silent (Hueter et al. et al. 2002). 2004). An exception is the cownose ray (Rhinoptera Other dipteran families with audible flight sounds and bonasus), which emits clicks in response to a human touch known pre-Cenozoic fossils include Bombyliidae (bee (Fish and Mowbray 1970). The cownose ray is a member flies), Tabanidae (horse flies), and bottle flies (Calliphor- of the family Myliobatidae, the earliest known members of idae). The oldest known members of Bombyliidae and which are from the latest Cretaceous (Campanian- Tabanidae are from the Lower Cretaceous, and the oldest Maastrichtian) (Cappetta 1987). known member of Calliphoridae is from the Upper Hearing has been demonstrated in Elasmobranchii Cretaceous (Blagoderov et al. 2002). In some dipterans, (sharks and rays) but has not been studied in Holocephali morphology and flight sounds mimic those of stinging (ratfishes). Elasmobranchs are known from as early as the hymenopterans, apparently to deter predators (Chapman Lower Devonian (Cappetta et al. 1993), so it is possible 1975). Such mimicry is unlikely to have arisen before the that anti-predator sounds directed at them existed by the appearance of stinging hymenopterans, which occurred in late Paleozoic. the Upper Jurassic (Grimaldi and Engel 2005).

Lobe-finned fishes (Osteichthyes: Sarcopterygii) Directions for further research Extant lungfishes (Sarcopterygii: Dipnoi) are generally Restudy of fossil insects – especially those that are well silent, although the Australian lungfish (Neoceratodus preserved in amber – to search for potentially overlooked forsteri) is known to breathe air noisily and to do it more bioacoustical structures might be worthwhile. A search for frequently during the breeding season, sometimes in stridulatory structures, highly sclerotised ventral surfaces concert in the evening (Kemp 1986). The sound is more (for percussion), and other sound-producing structures likely incidental than of use in intraspecific communi- could prove informative. Phylogenetic studies to deter- cation, because lungfishes lack specialisations for airborne mine homologies between sound-producing parts could be sound reception. Incidental air-breathing sounds that used to constrain phylogenetic levels at which homologous resemble whistling and clucking are also known in extant sound production occurred within given insect taxa, and salamanders (Maslin 1950), so the phenomenon is not fossils could then be used to constrain the times of origin limited to sarcopterygians outside Tetrapoda. Sarcopter- of such sounds. For this, a set of reliable phylogenies ygians are known from as early as the Upper Silurian incorporating these fossil taxa would be necessary to (Zhu et al. 2009), so the incidental sounds of air their determine historical homology as opposed to convergence. breathing may have existed that early. It would also be interesting to examine sound-producing and auditory parts of extant insects for correlations Ray-finned bony fishes (Osteichthyes: Actinopterygii) between morphology and dominant frequencies, and to apply the results to fossils to determine more precisely the Many actinopterygian taxa produce grunts, clicks, squeaks, nature of the sounds produced and heard by fossil insects whistles and other sounds for intraspecific communication (e.g. Rust et al. 1999). and when disturbed or apprehended (Fish and Mowbray 1970; Myrberg 1981; Ladich and Bass 2003). Such sounds

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 are typically produced by muscular vibration of the gas bladder, but in some species sound production is Pre-Cenozoic vertebrate paleobioacoustics accomplished by tendon snapping, pectoral girdle vibration, Non-bony fishes stridulation of pharyngeal teeth, or other methods (Ladich In vertebrates the inner ear exhibits a number of separate and Bass 2003). Actinopterygian acoustic behaviour has neuromast organs, some of which are used for 3D been studied mainly in teleosts (Teleostei). Not all teleosts orientation and some of which are used for sound reception are known to make sounds, and the variety of their sound (Ladich and Popper 2004). Sound reception has not been production mechanisms indicates that acoustic communi- demonstrated in the basal taxa Myxini (hagfishes) and cation evolved independently in several lineages (Schneider Petromyzontida (lampreys) but is present in Gnathosto- 1967; Ladich and Bass 2003). In addition to teleosts, mata (jawed vertebrates) (Ladich and Popper 2004). It may acoustic communication is known in basal ray-finned have appeared independently in cartilaginous fishes groups such as sturgeons (Acipenseridae) and bichirs (Gnathostomata: Chondrichthyes) and bony fishes (Polypteridae) (Johnston and Phillips 2003; Ladich and (Gnathostomata: Osteichthyes) because the former use a Bass 2003). Although the known fossil records of extant neuromast organ called the macula neglecta for hearing, ray-finned fish families that communicate acoustically go whereas in the latter the macula neglecta is reduced back no further than the Upper Jurassic (Table 5), those 270 P. Senter

Table 5. Families of sound-producing ﬁshes that are known from before the Cenozoic, and details about their sounds.

Family Earliest record Description of sound Function of sound Mechanism, if known Acipenseridae (sturgeons) Upper Cretaceous Squeak, chirp, knock, groan – – Albulidae (bonefishes) Upper Cretaceous Click, scratch, knock R – Ariidae (HS) (marine catfishes) Upper Cretaceous Grunt, creak, yelp R E Elopidae (tarpons) Upper Jurassic Thump R S Gadidae (cods) Upper Cretaceous Grunt A, C, G, R IN Holocentridae (HS) (squirrelfishes) Upper Cretaceous Staccato, grunt A, R, G E Myliobatidae (eagle rays) Upper Cretaceous Click R I Ophidiidae (cusk-eels) Upper Cretaceous – – – Polypteridae (bichirs) Upper Cretaceous Thump, moan A, R I

A, aggression; C, courtship; E, contraction of extrinsic swim bladder muscles; G, group coordination; HS, hearing specialist; I, sound produced by unknown internal mechanism; IN, contraction of intrinsic swim bladder muscles; R, response to predator, human touch, or startling; S, sound made by swimming. References: Myrberg 1981; Cappetta 1987; Ladich and Tadler 1988; Arratia 1993; Meunier and Gayet 1993; Nolf and Stringer 1993; Patterson 1993; Schwarzhans 1993; Stewart 1993; Johnston and Phillips 2003; Ladich and Bass 2003; Wilson et al. 2003. families phylogenetically bracket taxa from as early as the region of the inner ear is homologous in Anura and Amniota Upper Devonian (Carroll 1988; Grande and Bemis 1996). (Fritzsch 1992) but its coupling to a tympanum evolved The sounds of actinopterygian communication may there- separately in the ancestors of extant frogs, diapsids fore have existed through the late Paleozoic and Mesozoic. (Amniota: Diapsida) and mammals (Amniota: Mammalia) Basal ray-finned fishes must have been present by the (Bolt and Lombard 1985; Carroll 1991; Clack and Allin Upper Silurian, because Sarcopterygii, the sister taxon to 2004) (Figure 4). The earliest tetrapod skulls exhibit Actinpterygii, was present then (Zhu et al. 2009). The lungs posterior notches that are often called otic (ear) notches of extant basal actinopterygians may be homologous with because they superficially resemble the posterior skull those of lungfishes (Kardong 2006), in which case the notches that house tympana in extant frogs and amniotes. sound of noisy air-breathing by ray-finned fishes may have However, early tetrapod stapedial and otic morphology are existed alongside that of their lobe-finned counterparts as inconsistent with tympanic hearing (Clack et al. 2003). early as the Upper Silurian. The bony architecture of the notches indicates that they Underwater hearing is present in actinopterygians in housed spiracles, not tympana (Brazeau and Ahlberg 2006). general. A number of teleost taxa, known as hearing Even so, early tetrapod inner ears probably detected low- specialists, independently evolved connections between frequency water- and substrate-borne sounds, as do the the gas bladder and the inner ear (Ladich and Bass 2003). atympanic ears of extant fishes, salamanders and caecilians This increases the upper frequency range through which (Smotherman and Narins 2004; McCormick 1999; Ladich underwater sounds can be heard (Yan et al. 2000; Ladich and Bass 2003). and Bass 2003). Accordingly, sounds made by hearing The early tetrapod Ichthyostega exhibits otic modifi- specialist fishes are of higher frequency than those of other cations analogous to those of hearing-specialist fishes. fishes (Figure 3) (Ladich and Bass 2003). Hearing Uniquely among basal tetrapods, its skull appears to have specialist taxa include Otophysi (carp, catfishes and kin), had an air-filled otic chamber and a mobile stapes with a Anabantoidea (gouramis and kin), Mormyridae (mormyr- morphology and position conducive to sound conduction ids) and Holocentridae (squirrelfishes) (Ladich and Bass from the air-filled chamber to the inner ear (Clack et al. 2003). Hearing specialist fishes typically inhabit quiet, Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 2003). The otic chamber apparently functioned as a shallow water, which enhances high-frequency sound resonator for high-frequency sounds, as does the gas bladder transmission (Ladich and Bass 2003). It stands to reason, of hearing specialist fishes, which raises the possibility of then, that high-frequency acoustic behaviour of fossil high-frequency sonic communication in Ichthyostega. actinopterygians would have been more prevalent in quiet, Among members of Lissamphibia (the smallest clade shallow water than in noisy or deep water. The earliest including extant amphibians and all taxa phylogenetically known members of extant hearing specialist fish taxa are bracketed by them), tympanic ears are present in most extant from the Upper Cretaceous (Table 5). frogs (Anura) but are absent in basal frogs (Ascaphidae and Leiopelmatidae), caecilians (Gymnophiona) and salamanders (Caudata) (Bogert 1958; Smotherman and Narins Basal tetrapods (Tetrapoda) 2004). This suggests that the lissamphibian ancestor lacked In basal tetrapods a bone called the stapes served as a brace tympanic ears and that within Lissamphibia tympanic ears between the palate and braincase (Clack 1992). The stapes of are a synapomorphy of derived frogs. This interpretation is most extant frogs (Anura) and amniotes (Amniota) has been compatible with all three of the competing hypotheses of reoriented so that it couples the inner ear to a tympanum, lissamphibian origins. According to one hypothesis, enabling detection of airborne sounds. The sound-sensitive Lissamphibia arose from within the otherwise Paleozoic Historical Biology 271

clade Lepospondyli (Laurin and Reisz 1995, 1997, 1999; Laurin 1998; Vallin and Laurin 2004). According to the second hypothesis, Lissamphibia arose from within the otherwise mostly Paleozoic and Triassic clade Temnospon- dyli (Milner 1988; Trueb and Cloutier 1991; Ruta et al. 2003). According to the third hypothesis, frogs and salamanders arose from within tymnospondyli but caecilians arose from within Lepospondyli (Carroll 2007; Anderson et al. 2008). Lepospondyls show no osteological evidence of tympanic ears (Clack and Allin 2004). Many temnospondyls exhibit posterior cranial notches that have been interpreted as having housed tympana (Clack and Allin 2004). However, recent studies show that the morphology of the temporal area and the massive size of the stapes in temnospondyls are incompatible with the presence of a tympanum; the notches more likely housed spiracles (Laurin 1998; Laurin and Soler-Gijo´n 2006). The common ancestor of extant amphibians therefore lacked tympanic ears, regardless of which phylogenetic hypothesis is correct. Many large temnospondyls had large heads like those of extant crocodilians (Romer 1947), which acoustically advertise presence by slapping their heads on the water (Vliet 1989; Thorbjarnarson 1991; Thorbjarnarson and Herna´ndez 1993). It is therefore tempting to imagine large- headed temnospondyls employing the same communication device. Had they done so, their underwater hearing would have detected the sound and their lateral line systems (Romer 1947) would have detected the location of its source (Coombs and Braun 2003), even without tympana. However, the extreme proximity between shoulder girdle and skull in temnospondyls and other non-amniote tetrapods made the neck extremely short (Romer 1947), so it is unlikely that they could have raised their heads enough to have performed crocodilian-style head-slaps. This does not necessarily mean that extinct temnospondyls and other basal tetrapods were silent. It is possible that they performed other activities involving audible Figure 6. Estimated times of origin of sounds and tympanic ears water displacement. Also, several extant salamander in various animal lineages. See text for information sources. RPE, rampant parallel evolution of. species – which lack tympanic ears – produce airborne

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 anti-predator sounds in response to capture (Maslin 1950). Such defensive sound production may have evolved seymouriamorphs (Ivakhnenko 1987) (Figure 6), basal convergently in extinct basal tetrapods after the appear- tetrapod anti-predator sounds directed at ﬁshes may have ance of tympanic ears in their predators. Many extant existed before then. lissamphibians that make such sounds produce noxious Mechanisms of defensive sound production in extant chemicals that discourage or even kill predators (Duell- salamanders are listed in Table 6. Among extant salamander man and Trueb 1994). Others, such as amphiumas families, Cryptobranchidae (giant salamanders) and (Amphiumidae), can deliver a painful bite. Lissamphibian Amphiumidae (amphiumas) have a pre-Cenozoic fossil anti-predator sounds may therefore be honest warnings to record. The former are known from the Middle Jurassic of predators (Duellman and Trueb 1994), as is the case with China (Gao and Shubin 2003) and the latter from the Upper stridulating insects (Masters 1979). Noxious chemical Cretaceous of North America (Milner 1993). It is therefore production in extinct temnospondyls cannot be evaluated, possible that their characteristic defensive sounds existed but cranial and dental morphology of many temnospondyls before the Cenozoic. indicates the ability to produce a nasty bite, so they may Arthropod stridulation in response to seizure by have made honest warning sounds. While the earliest tetrapod predators began at the earliest in the Mississip- known predators with tympanic ears are Lower Permian pian, at which time the earliest insectivorous tetrapods 272 P. Senter

Table 6. Mechanisms of defensive sound production by extant salamanders (Maslin 1950).

Family Description of sound Mechanism (if known) Ambystomatidae (mole salamanders) Grunt------Laryngeal vocal cords Click, kissing sound------Forcefully opening mouth (sound produced by breakage of moist seal around mouth) Amphiumidae (amphiumas) Whistle, peep Forcing air through gill slits Cry similar to that of a – Cryptobranchidae (giant salamanders) human infant Dicamptodontidae (mole salamanders) Bark Laryngeal vocal cords Plethodontidae (lungless salamanders) Squeak – Proteidae (mudpuppies) Hiss – Forcefully opening mouth (sound produced by Salamandridae (newts and kin) Peep, squeak, kissing sound breakage of moist seal around mouth) Sirenidae (sirens) Croak, hiss –

appeared (Hotton et al. 1997). Mississippian tetrapods Tympanic ears and chorusing behaviour are present in lacked tympanic ears (see below) and therefore would the anuran clades Discoglossidae (midwife toads), have been deterred by the substrate-transmitted mechan- Mesobatrachia (spadefoot toads, clawed frogs and their ical vibrations produced by stridulation, rather than by the relatives) and Neobatrachia (typical frogs, tree frogs, true resulting sounds. Predator deterrence by airborne stridu- toads and their relatives), and therefore may be latory sounds would have been effective only after the symplesiomorphies of higher anurans. Discoglossoids appearance of tympanic ears in predatory tetrapods in the and mesobatrachians are known from Laurasia as early as Permian (see below). the Upper Jurassic (Henrici 1998) and from Gondwana as early as the Early Cretaceous (Baéz et al. 2000). Anuran chorusing therefore likely arose on those landmasses by Frogs (Lissamphibia: Anura) those times. The only known Mesozoic members of In lunged fishes, including lungfishes, the glottis (the Neobatrachia are South American members of Leptodac- opening in the pharynx that leads to the lung) is ringed by a tylidae from the Upper Cretaceous (Sanchiz 1998). muscular sphincter that closes the glottis (Negus 1949). Because no members of arboreal anuran clades are To this arrangement tetrapods have added the larynx known from the Mesozoic, we can safely infer that (Figure 1), an organ made of cartilage bodies (arytenoid Mesozoic anuran choruses took place at ground level. cartilages cranially and cricoid cartilages caudally) that During choruses, male anurans call to attract mates function as attachment sites for muscles that open the glottis (advertisement calls) and also emit special aggressive calls (Negus 1949; Kelemen 1963). In anurans paired vocal cords in response to the loud vocalisations of nearby male extend into the lumen from the arytenoid part of the larynx neighbours (Schwartz 2001). Aggressive calls may differ and are vibrated to produce vocalisation during forced qualitatively or quantitatively from advertisement calls expulsion of air from the lungs (Kelemen 1963), or during (Schwartz 2001). Females of many anuran species prefer inspiration in Bombina (Duellman and Trueb 1994). males whose calls are louder, delivered at higher rates, and

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 Members of Pipidae (clawed frogs) are exceptions; they delivered for longer periods; in fact, male anurans often lack vocal cords but produce a clicking noise by means of increase these parameters in their own calls in response to the sudden popping movement of a pair of articulating the calls of rivals (Schwartz 2001). If such directional cartilage disks attached to bony rods inside the larynx selection by female choice was present through anuran (Duellman and Trueb 1994). In most frogs, males possess a geological history, then Mesozoic anuran calls exhibited gular vocal sac that resonates and radiates the sound lower amplitude, rate and duration than extant anuran calls. (Duellman and Trueb 1994). During choruses, male frogs tend to vocalise during the Members of most families of anurans make anti- silences between calls of nearby conspeciﬁcs – or, for predator distress calls when disturbed (Bogert 1958). This species with multi-note calls, if the songs overlap, notes are is true even of basal taxa such as Leiopelma in which sung by one individual between the notes sung by another tympana, vocal sacs and courtship vocalisations are absent (Schwartz 2001). Such vocal alternation enables males to (Bogert 1958). Mesozoic anurans may therefore have detect each other’s calls and enables females to discriminate made anti-predator sounds before they acquired tympanic between individual males’ calls (Schwartz 2001). If vocal ears. Basal crown-group frogs are known from the Upper alternation during anuran chorusing evolved by means of Jurassic of Argentina (Henrici 1998), so anuran anti- directional selection, we can safely infer that it was absent predator sounds may have existed that early. or poor in the earliest anuran choruses. Historical Biology 273

Extinct basal tetrapods with tympanic ears Turtles (Reptilia: Testudines) Skull and the stapes morphology preclude tympana in Turtles and tortoises are usually silent but do occasionally most basal tetrapods, including basal amniotes (Reisz make sounds by unknown means. During copulation or 1981; Carroll 1991; Laurin 1998; Clack and Allin 2004; while chasing the female, males often make sounds that Laurin and Soler-Gijo´n 2006), but there were exceptions. have been described as grunts, groans, moans, bellows and A rodlike stapes oriented toward a strongly embayed roars (Gans and Maderson 1973; Auffenberg 1977). Such posterior skull notch suggests a tympanic ear in the Lower mating sounds are little studied but are known from such a and Upper Permian taxon Seymouriamorpha (Ivakhnenko wide taxonomic spectrum of turtle families (Campbell and 1987), which is phylogenetically intermediate between Evans 1972; Gans and Maderson 1973) that all extant turtles are phylogenetically bracketed by taxa known to Temnospondyli and Amniota (Laurin 1998; Laurin and produce mating sounds (Shaffer et al. 1997). This suggests Reisz 1999; Ruta et al. 2003) (Figure 4). A posterior skull that turtle mating sounds were present in the common embayment that suggests a tympanum is also present in the ancestor of crown group turtles, which appeared in the Upper Carboniferous and Lower Permian taxon Diadecto- Lower Jurassic (Rougier et al. 1995). Osteological morpha (Berman et al. 1992). Diadectomorpha is correlates of hearing in extant turtles are also present in phylogenetically positioned immediately outside Amniota the Upper Triassic and Lower Jurassic family Australo- (Laurin and Reisz 1995; Ruta et al. 2003) (Figure 4). chelidae, the sister taxon to the turtle crown clade A reduced stapes and a posterior skull embayment that (Gaffney and Kitching 1990). The situation is ambiguous suggest a tympanum are present in most members of in the Upper Triassic taxon Proganochelys, the most basal Parareptilia, a clade of dumpy-looking basal amniotes known fossil turtle, because of poor preservation in the from the Permian and Triassic (Carroll and Lindsay 1985; relevant region of the skull (Gaffney 1990). Laurin and Reisz 1995; Tsuji 2006; Mu¨ller and Tsuji The morphology of the tympanic region of the turtle 2007). The embayment is absent in Mesosauridae, the skull strongly resembles that of some parareptiles, and the most basal parareptilian group, and its presence is a same pair of bones (squamosal and quadratojugal) supports synapomorphy of higher parareptiles (Laurin and Reisz the tympanum in both groups (Carroll and Lindsay 1985; 1995; Tsuji 2006). Within Parareptilia the otic embayment Laurin and Reisz 1995; Rougier et al. 1995; Tsuji 2006). is particularly well developed in the Upper Permian and If turtles arose from within Parareptilia (Laurin and Reisz Triassic clade Procolophonoidea and a Middle Permian 1995; Lee 1997a,b), then the tympanic ears of turtles are clade informally called ‘nycteroleters’ (Carroll and probably homologous with those of parareptiles. This Lindsay 1985; Mu¨ller and Tsuji 2007). The orbits are introduces the possibility that parareptiles made turtle-like enlarged in both groups, suggesting crepuscular or courtship and mating sounds, in which case such sounds nocturnal habits, hence occupation of a visually compro- may have existed as early as the Permian. mised niche, to which the enhanced auditory apparatus While some phylogenetic analyses of morphological may be functionally related (Mu¨ller and Tsuji 2007). data place turtles within Parareptilia (Laurin and Reisz Taxa without tympanic ears ﬁll the phylogenetic gaps 1995; Lee 1997a,b), others place them just outside Diapsida between Seymouriamorpha, Diadectomorpha and Pararep- (Gauthier et al. 1988) or within crown Diapsida (Rieppel tilia, and also between these taxa and other amniote taxa and deBraga 1996; deBraga and Rieppel 1997). Curiously, with tympanic ears (Figure 4). Such ears therefore appeared molecular analyses usually place them within or closely independently in each group. The presence of tympanic ears related to the diapsid taxon Archosauria (Mannen et al.

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 in Seymouriamorpha, Diadectomorpha and Parareptilia 1997; Platz and Conlon 1997; Hedges and Poling 1999; made possible the use of airborne sounds in intraspeciﬁc Zardoya and Meyer 2001), for which there is no communication. However, there is no certainty that it documented morphological support, although one recent occurred. These groups may have used their tympanic ears molecular study places turtles in a phylogenetic position for other functions instead of (or in addition to) intraspeciﬁc compatible with parareptile status (Frost et al. 2006). If communication. Seymouriamorphs were carnivorous turtles are diapsids then their tympanic ears are homologous (Hotton et al. 1997) and may therefore have used hearing with those of other diapsids and not with those of to locate prey. A prey-locating function is unlikely in the parareptiles. largely herbivorous clades Diadectomorpha and Pararepti- lia. All three taxa may have used hearing for predator avoidance, as do extant reptiles (Greene 1988). Lizards and kin (Diapsida: Lepidosauromorpha) Lower Permian seymouriamorphs are the earliest Within the amniote taxon Diapsida are two major clades: known animals with tympanic ears that preyed on Lepidosauromorpha (lizards, tuataras and extinct kin) and vertebrates. The earliest airborne, anti-predator sounds Archosauromorpha (crocodilians, birds and extinct kin, made by vertebrates may therefore have been directed at including dinosaurs and pterosaurs) (Benton 1985) Lower Permian seymouriamorphs. (Figure 4). Extinct diapsids basal to the clade 274 P. Senter

Lepidosauromorpha þ Archosauromorpha lacked tympanic Marcellini 1977). Single chirps are used for threat calls ears (Reisz 1981; Clack and Allin 2004). Extant lepidosaur- (when lunging at a predator or conspecific rival) and omorphs and archosauromorphs possess tympanic ears, distress calls (upon being attacked or grasped), both in except for some in which tympanic ears have been lost: nocturnal and diurnal geckoes (Marcellini 1977). Tem- snakes (Serpentes), amphisbaenians (Amphisbaenia), Cali- porally patterned multiple chirps are used by nocturnal fornia legless lizards (Anniella), chameleons (Chamaeleoni- geckoes, usually males, in intraspecific social situations dae) and tuataras (Sphenodon) (Wever 1978). Most such (Marcellini 1977). Multiple chirps are produced at the groups are subterranean and therefore have no need for beginning of the nocturnal activity period, and may be airborne hearing (Wever 1978). While most extant snakes are uttered in response to other individuals’ calls, in response not subterranean, their ancestors probably were subterranean to the sight of rival males, and during courtship (Marcellini or aquatic (Apesteguıá and Zaher 2006; Palci and Caldwell 1977). Multiple chirp calls vary between species and 2007), so their lack of tympanic ears is a vestige of ancestry. appear to be related to spacing and territory (Marcellini Basal lepidosauromorphs and archosauromorphs exhi- 1977). The earliest known geckoes are from the Aptian- bit osteological evidence of tympanic ears (posteriorly Albian (Lower Cretaceous) of Mongolia (Alifanov 1989), embayed quadrate, thin stapes) (Gregory 1945; Robinson and it is possible that gecko calls were present then. 1962; Kuhn-Schnyder and Peyer 1973; Carroll 1975; The lepidosauromorph taxon Sphenodontia is today Gow 1975; Evans 1980; Dilkes 1998), which suggests represented by only one genus: Sphenodon (tuataras). inheritance from a common ancestor. A recently published Tuataras croak loudly when disturbed (Gans and Wever inference that the two lineages acquired tympanic ears 1976). Sphenodontians are known from as early as the separately is based on the assumption that the basal diapsid Upper Triassic (Fraser 1982). Sphenodon lacks tympana Youngina – which lacks evidence for tympanic ears – is a and has lost the embayment in the quadrate bone that is basal lepidosauromorph (Clack and Allin 2004). However, associated with the tympanum in lizards. The embayment recent phylogenetic analyses place Youngina outside the is present in basal sphenodontians (Evans 1980; Fraser lepidosauromorph-archosauromorph clade (Laurin 1991; 1982; Wu 1994) but was lost in the lineage leading to Rieppel and deBraga 1996; Lee 1997a,b; Modesto and Sphenodon by the Lower Jurassic (Reynoso and Clark Reisz 2002; Senter 2004). Enlarged orbits in basal 1998). The loss of tympanic ears indicates that the use of lepidosauromorphs and archosauromorphs (Robinson airborne sounds for intraspecific communication was not 1962; Kuhn-Schnyder and Peyer 1973; Carroll 1975; important in the lineage. Gow 1975; Evans 1980, Evans 1991; Modesto and Reisz Without tympanic ears extant tuataras have trouble 2002) suggest crepuscular or nocturnal habits, an hearing airborne sounds over 1 kHz but can hear their own interpretation supported by the fact that a reconstructed croaks, which are of appropriate frequency (Gans and ancestral archosaur visual pigment seems made for low Wever 1976) (Figure 3). Tuataras are not known to vocalise light levels (Chang et al. 2002). As with parareptiles for intraspecific communication, but the fact that they (Mu¨ller and Tsuji 2007), the enhancement of hearing in can hear their own voices suggests that they have the these animals may be functionally related to ancestral equipment with which to do so, even without tympanic ears. occupation of a visually compromised niche. This fact might tempt the researcher to conclude that basal, The earliest known lepidosauromorphs and archosaur- terrestrial tetrapods without tympanic ears may have used omorphs are from the Upper Permian (Carroll 1975; Evans low-frequency vocalisations for intraspecific communi- and King 1993). Whether or not the two groups acquired cation. However, such temptation should be resisted.

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 airborne hearing independently, it was present in both by The loss of the tympanum in extant reptiles results not only then. Anti-predator sounds directed at diapsids may in a limitation of auditory sensitivity to low-frequency therefore have appeared in the Upper Permian. The small, sounds (Figure 3), but also results in an inability to hear peglike teeth of many basal diapsids, including basal such sounds except at very high amplitudes (Wever 1978). lepidosauromorphs and basal archosauromorphs, suggest Snakes are exceptions to this rule, because they can hear a diet of invertebrates (Colbert 1970; Carroll 1975; low-frequency sounds at low amplitudes (Wever 1978). Gow 1975; Evans 1980). Anti-predator sounds directed at However, the example of the snake’s ear is inapplicable to Permian diapsids may therefore have included stridulation basal tetrapods, for two reasons. First, the quadrate bone of by arachnids and beetles. a snake’s skull (Figure 1) is so loose that it vibrates The ability to hear airborne sounds allows acoustic freely and has essentially become a bony tympanum communication, but among extant lizard families with (Wever 1978), whereas no posterior skull bone was loose in Mesozoic records only geckoes (Gekkonidae and Euble- basal tetrapods. Second, the stapes of a snake is slender and pharidae) vocalise. Using laryngeal vocal cords, geckoes contacts the quadrate as if contacting a tympanum (Wever make sounds that are described as squeaks, growls and 1978) (Figure 1), whereas the basal tetrapod stapes was a barks, which carry only for a few meters in some cases and robust, solid brace between the bones of the cheek or palate as far as 20 m in others (Gans and Maderson 1973; and the braincase (Carroll 1986; Clack 1992). Historical Biology 275

Mesozoic marine reptiles – and pterosaurs (Pterosauria) and a few other extinct Stapedial and posterior skull morphology indicate forms (Sereno 1991). The vocal organ in extant members retention of tympanic ears in Nothosauria, a marine of Crurotarsi (crocodilians) is the larynx, whereas in extant archosauromorph clade from the Triassic Period members of Ornithodira (birds) it is the syrinx. Because (Carroll and Gaskill 1985). This indicates an ability to the larynx and syrinx are not homologous, it is most hear airborne sounds in these animals, despite their aquatic parsimonious to infer that vocalisation arose indepen- habits. In Plesiosauria, a Mesozoic marine taxon closely dently in the two lineages, in which case their common related to Nothosauria, a thin stapes suggests evolution ancestor lacked vocal ability. from an ancestor with tympanic ears (Hetherington 2008). Crocodilians vocalise by vibrating three mucosal However, posterior skull morphology indicates that the folds – absent in the avian larynx (McLelland 1989a,b) – tympanum was lost in Plesiosauria (Carpenter 1997; that project into the laryngeal lumen under part of the Storrs 1997; Hetherington 2008). arytenoid cartilage (Reese 1914). Unlike the avian syrinx A tympanic notch is absent in the Mesozoic marine (see below), the crocodilian vocal organ leaves no trace of taxon Ichthyosauria (Maisch 1997), which may or may not its presence on fossil skeletons, so it is impossible to know be a member of Diapsida (Maisch 1997; Motani et al. whether vocalisation was present further down the 1998). The ichthyosaur stapes is robust and serves as a crurotarsian tree than Crocodylia. We therefore cannot brace between the cheek and braincase (Hetherington know whether the Triassic and Jurassic Periods were filled 2008), as in basal amniotes (Clack and Allin 2004). This with the roaring of basal crurotarsians. suggests that ichthyosaur ancestors never passed through a On the other hand, we can infer that the homologous stage with tympanic ears. The lack of tympanic ears in acoustic behaviours of gharials (Gavialidae), crocodiles plesiosaurs and ichthyosaurs does not necessarily mean (Crocodylidae), alligators and caimans (Alligatoridae) that they were deaf to underwater sounds but does indicate were present in their common ancestor (Senter 2008), a lack of importance of airborne sounds to them. which appeared in the Upper Cretaceous (Brochu 2003). Mosasauridae, a marine family of Upper Cretaceous Juvenile crocodilians of all three groups squeak or grunt lizards, retained tympanic ears, but they were modified for when disturbed, sometimes even from within the egg if the underwater sound reception. The tympanum was often nest is disturbed, and the sound attracts adults ossified, increasing resistance to rupture in deep water (Modha 1967; Whitaker and Basu 1982; Cintra 1989; (Russell 1967). The middle ear cavity was encased in bone Whitaker and Whitaker 1989). Adult males of all three and lacked acoustic isolation from the rest of the skull, groups engage in head-slapping, in which the head is allowing the skull to conduct sound to the middle ear raised and then slammed downward onto the water’s (Hetherington 2008). Underwater hearing was therefore surface to create a loud splash that is often followed by a apparently important to mosasaurs. It is impossible to hiss in gharials or a roar in alligators and crocodiles know, however, whether mosasaur hearing was of (Garrick et al. 1978; Whitaker and Basu 1982; importance in prey localisation, avoidance of dangerous Thorbjarnarson 1991; Thorbjarnarson and Hernańdez animals emitting honest sonic warnings, intraspecific 1993). The head-slap is used in displays of presence and communication, or a combination of factors. dominance and in courtship (Garrick et al. 1978; Thorbjarnarson 1989; Whitaker and Whitaker 1989). Courtship in gharials, alligators and crocodiles also Crocodilians and kin (Archosauromorpha: Archosauria: involves geysering (shooting jets of water upward from Crurotarsi) Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 the nostrils, which are held just below the surface) and Basal diapsids appear to have been insectivorous, but the blowing bubbles in the water with the mouth (Garrick et al. serrated, ziphodont teeth of the archosauromorph clade 1978; Whitaker and Basu 1982; Thorbjarnarson 1989; Archosauriformes indicate a switch to a diet of vertebrates Whitaker and Whitaker 1989; Thorbjarnarson and (Senter 2003). Archosauriformes exploded in diversity in Hernańdez 1993). Narial geysering is also used as a the Triassic Period but at least one of its basal members territorial display (Modha 1967; Garrick et al. 1978). was present in the Upper Permian (Hughes 1963). Anti- Territorial fights between crocodilian males often involve predator sounds from vertebrates, directed at archosauri- loud splashing as bodies are hurled against each other forms, may therefore have been present that early. (Modha 1967; Singh and Rao 1990). Members of Archosauria, the archosauriform crown The above are all water-based behaviours that would clade, are known from as early as the Middle Triassic obviously have been absent in the terrestrial precursors of (Sereno 1991). Archosauria includes two major lineages, Crocodylia. Aquatic or semi-aquatic habits are character- Crurotarsi and Ornithodira (Sereno 1991) (Figure 4). istic of a large clade, Neosuchia, which includes Crurotarsi includes crocodilians (Crocodylia) and several Crocodylia and several extinct Mesozoic taxa extinct, mostly Triassic taxa (Sereno 1991). Ornithodira (Clark 1994). If the aquatic acoustic behaviours of includes dinosaurs (Dinosauria) – including birds (Aves) crocodilians were present further down neosuchian 276 P. Senter

phylogeny, they may have been present as early as the avian clade Ornithothoraces – which includes modern Upper Jurassic, from which the earliest non-marine birds and the Lower and Upper Cretaceous taxon neosuchians are known (Carroll 1988). Enantiornithes (Chiappe and Walker 2002) – but not in Most phylogenetic analyses place the marine taxon birds basal to Ornithothoraces (Chiappe et al. 1999; Zhou Thalattosuchia within Neosuchia (e.g. Clark 1994; Ortega and Zhang 2003). et al. 2000; Sereno et al. 2001; Company et al. 2005). The clavicular air sac does not develop individually Thalattosuchians, known from as early as the Lower but instead represents a fusion of outgrowths from two pre- Jurassic (Carroll 1988), had narrow snouts (Clark 1994). existing air sacs and a pair of outgrowths from the lungs. Thalattosuchian head-slapping, if it occurred, would The four outgrowths do not meet in the midline, in the therefore have been weak for the sake of protecting the vicinity of the syrinx, until late in embryology (Locy and narrow snout, as in the extant gharial (Whitaker and Basu Larsell 1916). The status of the clavicular air sac as an 1982). Snouts were wider in most other extinct outgrowth of pre-existing structures, two of which are neosuchians (Clark 1994), allowing strong head-slaps. other air sacs, suggests that it is a later evolutionary Head-slaps, if present, would have been particularly acquisition than the original set of ornithodiran air sacs. impressive in the gigantic taxa Sarcosuchus and Deino- This is consistent with the interpretation that it arrived suchus, in each of which head length approached 2 m relatively late in ornithodiran history. Evidence exists that (Sereno et al. 2001; Schwimmer 2002). Sarcosuchus is a non-avian ornithodirans, including basal birds, possessed neosuchian from the Lower Cretaceous (Aptian-Albian) of other air sacs homologous with those of birds (Britt et al. western Africa (Sereno et al. 2001), and Deinosuchus is an 1998; O’Connor 2006; Wedel 2006), but not the clavicular alligatoroid from the Upper Cretaceous (Campanian) of air sac. Outside Ornithothoraces, humeral pneumatisation North America (Schwimmer 2002). Deinosuchus is more is present in Pterosauria (O’Connor 2006) but not in the certain than Sarcosuchus to have employed head-slapping many intervening dinosaurian taxa (Britt 1997). Humeral behaviour because Deinosuchus lies within Crocodylia pneumatisation in pterosaurs is therefore not homologous (Sereno et al. 2001), whereas Sarcosuchus does not (Sereno with that of birds and so is not evidence for the presence of et al. 2001). Also, Sarcosuchus is phylogenetically a clavicular air sac homologous with that of birds. bracketed by narrow-snouted forms (Sereno et al. 2001), Pneumatisation of the furcula is present in the allosauroid which increases the likelihood that head-slapping beha- theropod Aerosteon riocoloradensis, suggesting the pre- viour, if present that far back in neosuchian phylogeny, was sence of a clavicular air sac (Sereno et al. 2008). However, lost or weakened in the clade that includes Sarcosuchus. such a sac is not likely homologous with that of Members of Alligatoridae (alligators and caimans) ornithothoracine birds because its osteological indicator employ both head-slapping and a vocal acoustic advertise- (furcular pneumatisation) is absent in phylogenetically ment display called bellowing (Garrick 1975; Garrick et al. intermediate taxa, including other allosauroids (Chure and 1978; Gorzula and Seijas 1989).Maleand femalealligatorids Madsen 1996), basal birds (Chiappe et al. 1999; Zhou and bellow to advertise presence. Bellowing is contagious and its Zhang 2003; Mayr et al. 2007) and non-avian coelur- sound is sexually dimorphic (Garrick 1975; Garrick et al. osaurian theropods (Norell et al. 1997; Makovicky and 1978). Alligatoridae is unknown before the Cenozoic Currie 1998; Clark et al. 1999; Xu and Norell 2004). (Brochu 2003), but other members of Alligatoroidea, the Without evidence for a clavicular air sac homologous with larger taxon that includes Alligatoridae but excludes that of birds, we should not presume that basal birds and Crocodylidaeand Gavialidae,werepresentinNorth America non-avian ornithodirans possessed a functioning syrinx.

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 as early as the Campanian (Upper Cretaceous) (Brochu The lack of evidence of a syrinx in ornithodirans 1999). If basal alligatoroids bellowed, then the sound may outside Ornithothoraces will, no doubt, disappoint fans of have been present in the Upper Cretaceous. roaring movie dinosaurs. However, lack of ability to vocalise does not necessarily mean that such animals were silent altogether. Many extant reptiles communicate with Birds and kin (Archosauria: Ornithodira) each other and with potential predators by non-vocal The syrinx of birds (Ornithodira: Aves) is a series of acoustic means such as hissing, clapping jaws together, cartilage rings at the junction of the trachea and primary grinding mandibles against upper jaws, rubbing scales bronchi, with membranous folds that protrude into the together, or use of environmental materials (e.g. splashing lumen and can be vibrated to produce sound (Brackenbury against water) (Campbell and Evans 1972; Gans and 1989; King 1989). Vocal production by the syrinx depends Maderson 1973; Garrick et al. 1978; Thorbjarnarson and on the presence of a clavicular air sac (Brackenbury 1989), Herna´ndez 1993). Birds also use non-vocal acoustic means a soft structure that invades and pneumatises the bones of of communication such as hissing, bill-clapping, stamping the avian pectoral girdle and limb, marking its presence and wing beating (Welty and Baptista 1988; Kear 2005; with a characteristic opening on the humerus (McLelland Nelson 2005). Non-avian theropods with feathered wings 1989a,b). Such an opening is present in members of the may have beaten their wings in acoustic displays as extant Historical Biology 277

birds often do. Sauropod dinosaurs of the family contact calls suggests that they may be behavioural Diplodocidae, known from the Upper Jurassic of North symplesiomorphies for Galloanserae and therefore were America and Africa (Upchurch et al. 2004), possessed present in the Cretaceous. whiplike tail tips that could have produced loud, whiplike Members of Gaviiformes (loons) are known from the cracking sounds for intraspecific communication or in latest Cretaceous (Maastrichtian) of South America (Hope response to predators (Myhrvold and Currie 1997). 2002). Loons emit trains of clucking sounds during flight The morphology of the nasal passage in Lambeosaur- and a variety of calls in other situations (Oberholser 1974). inae, a Laurasian clade of Upper Cretaceous ornithischians Far-reaching, drawn-out advertisement calls known as (Horner et al. 2004), suggests a role in sonic resonation wails or yodels are produced at dawn and dusk during the (Weishampel 1981). However, resonation need not be for breeding season (Oberholser 1974). In most loons takeoff vocal sounds. Some extant snakes lack vocal cords but involves much noise because a loon has to run along the possess resonating chambers that emphasise the low water’s surface for a long distance to become airborne, and frequencies of the hiss (Young 1991). The variety of visual landing may involve a powerful splash (Oberholser 1974). display structures in pterosaurs and dinosaurs (Chapman Members of the extant family Phalacrocoracidae et al. 1997; Molnar 2005; Unwin 2006) shows that visual (cormorants, order Pelecaniformes) are known from the communication was important to these animals. They may latest Cretaceous (Maastrichtian) of Asia and North therefore have relied largely on visual means of America (Hope 2002). Several acoustic characteristics and communication. Extant precedent for such reliance is behaviours found in cormorants are widespread in found among lizards, in which non-chemical communi- Pelecaniformes and may be behavioural symplesiomor- cation is primarily visual (Pough et al. 1998), despite their phies for the group. These include general silence away excellent hearing (Wever 1978). from the nesting colony except for loud communal fishing Members of a few extant bird orders are known from calls; high-pitched begging calls from chicks; sexual before the Cenozoic. Members of Anseriformes (water- dimorphism in voice; emission of hisses and special fowl) are known from the latest Cretaceous (Campanian- disturbance calls during nest-usurpation attempts; copula- Maastrichtian) of Asia, North America and Antarctica tory vocalisations and the ability to recognise the voices of (Hope 2002; Clarke et al. 2005). Several acoustic offspring and neighbours (Nelson 2005). Other acoustic behaviours are taxonomically widespread within Anser- characteristics that are typical of cormorants but not other iformes and may be behavioural symplesiomorphies of the pelecaniformes include squeaky complaint calls from group: near-constant contact calls of low amplitude among chicks when disturbed; loss of the female voice after five groups, pairs or parents and offspring; a loud duet called a to six weeks; growling or loud barks by males in nest triumph display by a pair after an agonistic encounter; a defense; and a display by the male when advertising for a special greeting call; a special post-copulatory call; a female in which he throws his head back and makes special alarm call; calling during takeoff and throughout neighing or gargling sounds and follows this with ‘Goww, flight; defensive hissing and among juveniles, special gow, goww,’ if the female approaches (Nelson 2005). distress calls, begging calls and calls expressing sleepiness Some fragmentary Upper Cretaceous (Maastrichtian) (Kear 2005). Vocal pitch usually differs between the sexes bird specimens have been referred to Charadriiformes and is higher in juveniles than adults (Kear 2005). (shorebirds) and Psittaciformes (parrots), but these Members of Galliformes (game birds) are known from assignments are doubtful (Hope 2002). We therefore the latest Cretaceous (Campanian-Maastrichtian) of North cannot confidently infer that typical shorebird or parrot

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 America (Hope 2002). Several acoustic behaviours are calls were present before the Cenozoic. taxonomically widespread within Galliformes and may be Among extant birds, the vocabularies of basal groups – behavioural symplesiomorphies of the group: frequent ratites, tinamous, waterfowl, and galliforms – tend to be utterance of contact calls of low pitch and amplitude differentiated at least into loud advertisement calls, soft among aggregations and pairs; a loud, far-carrying, often contact calls, special alarm calls, and (in Ratitae and multi-syllable advertisement call by the male that is often Anseriformes) the use of hissing as a threat (Jones et al. answered by the female to form a vocally dimorphic duet 1995; Davies 2002; Madge and McGowan 2002; Kear that may be answered by neighbouring males or pairs; a 2005). Such differentiation also occurs in more derived special alarm call; and a loud, rapid, multi-syllable call groups (e.g. Nelson 2005) and therefore may be that differs from the usual alarm call, upon takeoff when symplesiomorphic for Neornithes, the clade that includes ﬂushed (Jones et al. 1995; Madge and McGowan 2002). all birds phylogenetically bracketed by the extant bird Anseriformes and Galliformes together form the clade orders. The earliest known neornithean birds are from the Galloanserae, which is the sister clade to all other extant Upper Cretaceous (Campanian) (Hope 2002), at which birds except ratites and tinamous (van Tuinen et al. 2000). time the differentiation was probably present. The frequent occurrence in both Anseriformes and Extant bird vocalisations vary in pitch according to body Galliformes of duetting and near-constant, low-amplitude size, with smaller birds emitting vocalisations of higher 278 P. Senter

frequency (Welty and Baptista 1988). Avian body size is quadrate such as diapsids possess (Luo and Crompton also correlated with the range of frequencies detectable by 1994). Some researchers have suggested that a mandibular the inner ear, with smaller birds capable of detecting higher tympanum was present in derived Permian and Triassic frequencies (Gleich et al. 2004). There is no reason to expect synapsids with a posterior mandibular cleft bordered by that the same was not true of Mesozoic birds. bones homologous to those that contact the mammalian Whether or not Mesozoic birds sang is at least partly a tympanum (e.g. Allin 1986). However, three lines of semantic issue. According to the technical definition, an evidence support the absence of a tympanum outside a avian advertisement call is considered a ‘song’ if it is derived synapsid clade that appeared in the Upper Triassic. acoustically complex, multi-syllabic, and exhibits shorter That clade, hereafter called the DS (derived synapsid) clade pauses between notes than the pauses between groups of for concision, includes mammals and their extinct outgroups notes (Welty and Baptista 1988). In practice, however, Morganucodontidae and Tritylodontidae (Figure 4). First, avian advertisement vocalisations are called ‘songs’ if they the synapsid homologue of the cochlea retained its issue from the mouths of songbirds (Passeriformes), doves plesiomorphic, globular shape in other synapsids (Allin (Columbiformes) or tinamous (Tinamiformes), whether or 1986) but became elongated, indicating increased auditory not they are complex or multi-syllabic. This is probably acuity, in the DS clade (Vater et al. 2004). Second, because the advertisement vocalisations of these taxa have a osteological evidence suggests that the posterior mandibular quality that is musical to human ears. The less pleasant (to bones were muscle attachment sites in other synapsids but humans) advertisement vocalisations of other bird taxa are not in the DS clade, and the attachment of muscles would considered ‘calls’ rather than ‘songs,’ despite their similar have impeded transmission of vibrations from a tympanum function and the fact that in some taxa (e.g. galliforms and (Kemp 2005). Third, the attachment of the posterior loons) they fit the technical definition of ‘song.’ In any case, mandibular bones was solid, impeding transmission of Mesozoic bird sounds probably lacked musical quality vibrations from a tympanum, in other synapsids but was because songbirds, doves and tinamous lack Mesozoic loose, facilitating transmission of vibrations, in the DS clade records (Unwin 1993; Boles 1995), and musical vocalisa- (Crompton and Hylander 1986). tions are not the norm in other birds. The same three lines of evidence also suggest an increase in auditory acuity at the base of the DS clade. However, they do not demonstrate the presence of Mammals and kin (Amniota: Synapsida) tympana. New osteological evidence from a particularly The amniote clade Synapsida includes mammals (Mam- well-preserved skull of Chiniquodon, a non-mammalian malia) and their extinct relatives. Basal synapsids member of the DS clade, shows that the posterior (‘pelycosaurs’) lacked tympanic ears (Carroll 1986). The mandibular bones were acoustically isolated from the bones that support the tympanum in mammals and connect anterior mandible and were free to vibrate as a unit about it with the stapes are homologous to the posterior bones of their collective longitudinal axis in response to low- the mandible and jaw joint in other synapsids (Allin 1986; frequency airborne sound (Kemp 2007). However, the Luo and Crompton 1994). In the synapsids most closely arrangement of the rest of the skull bones precludes the related to mammals these bones became smaller and less presence of an air-filled tympanic cavity, without which a solidly attached to the anterior mandible (Allin 1986; tympanum is pointless (Kemp 2007). Basal members of Crompton and Hylander 1986). In basal mammals – and the DS clade could therefore hear airborne sounds but only possibly in Hadrocodium, the genus most closely related to at low frequencies (Kemp 2007).

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 mammals (Luo et al. 2001) – these bones detached from Extant mammals of all three clades – Monotremata the mandible and became incorporated into the middle ear (egg-laying mammals: echidna and platypus), Metatheria (Wang et al. 2001). This specialisation was present by the (marsupials) and Eutheria (placental mammals) – vocalise Middle Jurassic at the latest (Kielan-Jaworowska et al. using vocal cords in the larynx. Their common ancestor, 2004), and by the Lower Jurassic if it was present in which appeared in the Middle Jurassic (Kielan-Jawor- Hadrocodium (Luo et al. 2001). It indicates deﬁnitive owska et al. 2004), therefore presumably also could evidence for tympanic hearing, hence the possibility of vocalise with laryngeal vocal cords. It is uncertain how acoustic communication, in the earliest mammals. The much, if any, further back in synapsid phylogeny vocal earliest mammals and their predecessors were probably cords were present. Venomous hindlimb spurs are nocturnal (Crompton et al. 1978), so their evolution of plesiomorphic for the clade that includes Mammalia and airborne hearing may have been functionally related to its close outgroup Docodonta (Hurum et al. 2006), which their occupation of a visually compromised niche. phylogenetically bracket Lower Jurassic taxa (Kielan- The possibility of tympanic hearing in synapsids Jaworowska et al. 2004). If proto-mammals employed intermediate between ‘pelycosaurs’ and mammals has acoustic ‘honest warnings’ to predators, as do many received attention. There are strong osteological indicators insects and amphibians (Masters 1979; Duellman and that these animals lacked a tympanum posterior to the Trueb 1994), vocal cords may have been present as far Historical Biology 279

back as the common ancestor of Docodonta and Also, the possibility of behavioural homology of defensive Mammalia in the Lower Jurassic. hissing in marsupials and reptiles suggests that hissing was In monotremes and the extinct basal mammalian clade a typical defensive behaviour through the synapsid Multituberculata, the cochlea is more elongated than in ancestry of mammals. more basal synapsids, indicating that a wider range of In placental mammals the thyroid cartilage has detached frequencies can be heard; even so, monotreme auditory from the cricoid cartilage (Figure 1) and the laryngeal acuity is poor, with a peak at 5 kHz and low ability to hear musculature is elaborated, so the eutherian larynx facilitates low-amplitude sounds (Vater et al. 2004). Therefore, in more elaborate vocalisation than is possible in monotremes Mesozoic mammals of this grade, any vocalisations used in and marsupials (Kelemen 1963). Perhaps because of this the intraspecific communication likely exhibited low pitch. vocabularies of placental mammals tend to be larger than In contrast, the cochleae of therian (marsupial and placental) those of monotremes and marsupials and can convey mammals are extremely elongated and coiled, allowing information about a wider variety of situations and hearing through wide frequency ranges even at low emotional states (Estes 1991). The earliest known placental amplitudes (Vater et al. 2004). The frequencies of peak mammals are from the Lower Cretaceous (Barremian) sensitivity for therian ears vary inversely according to body (Ji et al. 2002), and complex vocabularies may have existed size, with the largest therian ears sensitive to infrasound and among placentals that early. the smallest sensitive to ultrasound (Long 1994) (Figure 1). One extant placental order, Soricomorpha (shrews, Therefore, in Mesozoic therians, vocalisations used in tenrecs, hedgehogs and kin), is known from the Mesozoic intraspecific communication likely were of highest pitch in (Kielan-Jaworowska et al. 2004). Echolocation, clicking small species and of lower pitch in larger species. sounds, defensive hissing and aggressive squeaking are The monotreme and marsupial vocal apparatus is poor, common and taxonomically widespread in extant sorico- due to fusion of the thyroid cartilage (a mammalian morphs (Nowak and Paradiso 1983). If these are ancestral apomorphy) of the larynx with the cricoid cartilage and the acoustic behaviours for Soricomorpha, they were present possession of primitive laryngeal musculature (Negus 1949; before the Cenozoic. Soricomorphs are known from as Kelemen 1963). Perhaps because of this, monotreme and early as the Coniacian (Upper Cretaceous) of Asia and the marsupial vocal sounds are generally simpler than those of Campanian (Upper Cretaceous) of North America placental mammals, and their vocabularies are smaller. (Kielan-Jaworowska et al. 2004). Cooing, purring and snuffing sounds of unclear significance Other extant placental orders are unknown before the are known in echidnas (Tachyglossidae) (Hutchins 2004). Cenozoic, but members of some extant placental supraor- Platypuses (Ornithorhynchus) growl when disturbed, and dinal taxa are present. Basal members of Archonta, which the female emits pre-copulatory squeaks that are answered includes the orders Dermoptera (colugos), Chiroptera (bats) by the male; juveniles make squeaking contact calls to each and Primates (primates), are known from the latest other during play and are also known to hiss (Tembrock Cretaceous (Maastrichtian) of India (Kielan-Jaworowska 1963; Griffiths 1978). Marsupial vocabularies often include et al. 2004). Basal members of the supraordinal taxon courtship vocalisations, aggressive vocalisations, and Ungulatomorpha (hoofed mammals) are known from as hissing as a defensive sound, although in some taxa early as the Upper Cretaceous (Turonian) of Asia and the defensive sounds are vocal (Nowak 2005). More extensive latest Cretaceous (Campanian-Maastrichtian) of Europe and vocabularies exist in the marsupial genus Macropus (true South America (Kielan-Jaworowska et al. 2004). Sounds kangaroos), but this is probably related to eusociality, a trait made by extant archontans and ungulatomorphs are too

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 characteristic of Macropus and uncharacteristic of marsu- varied across taxa (Hill and Smith 1984; Estes 1991) to infer pials in general (Menkhorst and Knight 2004). It is therefore ancestral acoustic behaviour for either group. Basal doubtful that complex vocabularies existed among Meso- members of Ferae, which includes the order Carnivora zoic marsupials. and a few extinct orders, are known from the latest Stem-group marsupials are known from as early as the Cretaceous (Campanian-Maastrichtian) of North America Lower Cretaceous (Aptian-Albian) (Kielan-Jaworowska (Kielan-Jaworowska et al. 2004). Sounds made by extant et al. 2004), but no member of the marsupial crown group carnivorans vary, but three types of sounds are common to is known from before the Cenozoic (Rougier et al. 1998). so many members of so many carnivoran families that they None of the vocalisations characteristic of extant may be plesiomorphic for Carnivora or perhaps even Ferae: marsupial families can therefore be inferred to have low-pitched growling to communicate threat, high-pitched existed before the Cenozoic. However, the fact that vocalisations in response to physical pain, and high-pitched vocabularies are differentiated into different vocalisations distress and contact calls from juveniles (Estes 1991). for different situations in both platypuses and marsupials Drumming with the hind feet on the substrate is a suggests that such differentiation is an ancient trait. Vocal common method to communicate alarm or the presence of differentiation may therefore have been present in the danger among mammals with hindlimbs that are specialised common mammalian ancestor in the Middle Jurassic. for saltatory locomotion (hopping). This method has 280 P. Senter

appeared convergently in Macropodidae (kangaroos and In addition to such tidbits, a larger paleobioacoustical their saltatory relatives), Macroscelididae (elephant scenario emerges from the pooled information presented shrews), Leporidae (rabbits), Dipodidae (jerboas) and here (Figure 6). Incidental animal sounds were probably Dipodomys (kangaroo rats) (Nowak and Paradiso 1983; present in the oceans by the beginning of the Paleozoic Menkhorst and Knight 2004). It is probably no coincidence Era, but those sounds were not heard (except perhaps by that this form of communication is prevalent among cephalopods) until much later. The first terrestrial mammals of this morphotype and that in all cases it arthropod communities arose in the Silurian Period, and transmits the same type of information. Theoretically, a defensive stridulation in terrestrial arthropods may have novel reflexive behaviour in response to a given stimulus appeared soon thereafter. In the Silurian Period cartilagi- could most easily evolve by modification of a preexisting nous and bony fishes appeared, and each independently reflexive behaviour involving the same set of muscles in acquired the ability to hear low-frequency water-borne response to the same stimulus. An oscillatory hindlimb sounds. Parallel evolution of defensive, aggressive and motor reflex (drumming) in response to danger might courtship sounds is rampant among ray-finned fishes and therefore most easily evolve in mammals that already have a may have begun in the Silurian or Devonian. Malacos- preexisting oscillatory hindlimb motor reflex (hopping) in tracan crustaceans also appeared in the Devonian, and response to danger. Because of its prevalence among several lineages evolved defensive stridulation in parallel, saltatory mammals, it is possible that this method of possibly in response to predation by fishes with underwater acoustic communication of alarm/danger was present in hearing. Bony fishes and early tetrapods of the Silurian and Zalambdalestes, a saltatory placental mammal from the Devonian Periods engaged in noisy air-breathing without Upper Cretaceous (Campanian) of Mongolia (Kielan- fear of being overheard by predators, because no Jaworowska 1978). vertebrate had yet acquired tympanic ears. Tetrapods exploded in diversity in the Carboniferous Period. Amniotes appeared in the Pennsylvanian and Directions for further research employeddefensive displaysthat incorporatedbodyinflation as a visual signal. The resulting hissing sound was first heard Rigorous analysis is needed to determine whether the by seymouriamorph predators in the Lower Permian and by potential acoustic behavioural homologies proposed here archosauriform predators in the Upper Permian. Arthropod within Aves and Mammalia meet tests of homology. It defensive stridulation was heard by diapsid predators for the would also be informative to compare aspects of first time in the Upper Permian, although the mechanical vocalisation across anuran, avian and mammalian vibrations produced by stridulation may have deterred other phylogeny to determine whether or not it is possible to tetrapod predators as early as the Mississippian. infer ancestral characteristics of vocal sounds in each An explosion of terrestrial sound appeared in the group. It would also be informative to study inner ear Triassic Period. Low-frequency twilight choruses may endocasts of more fossil archosaurian and synapsid taxa to already have existed among ray-finned fishes, but the determine hearing ranges, as has been done for a few taxa earliest terrestrial twilight choruses appeared in the Triassic (Gleich et al. 2004; Vater et al. 2004). In addition, it would with the advent of crickets and their mesoedischiid and be interesting to study sound-producing structures across titanopteran relatives. The drumming of stoneflies appeared the phylogeny of ray-finned fishes to determine whether in the Middle Triassic. The hemipteran taxon Prosorrhyncha homologies in acoustic anatomy can be assessed. appeared in the Upper Triassic and radiated into several

Downloaded By: [Canadian Research Knowledge Network] At: 16:50 18 September 2009 lineages that evolved defensive and courtship stridulation in parallel. Turtles first appeared in the Upper Triassic; their The big picture courtship sounds may have appeared soon thereafter, or The evidence and inferences presented above suggest that those sounds may be evolutionary continuations of court- the questions posed in this paper’s opening paragraph can ship sounds that were present in parareptiles from perhaps as be answered. Triceratops and indeed even the earliest early as the Permian. dinosaurs heard crickets chirping in the evening. Water boatmen joined the twilight chorus in the Lower The Mesozoic treetops did not resound with frogsong, Jurassic, and anurans joined it in the Upper Jurassic. although Upper Jurassic and Cretaceous bodies of water Venomous mammals began making defensive vocalisa- did. Cretaceous treetops were filled with the sounds of tions in the Lower Jurassic. Tympanic ears appeared in honking, cackling and wailing birds in what must have mammals by the Middle Jurassic and may have been used been an awful cacophony that would not become sweet to locate (chorusing?) insect prey. The tapping of booklice, and musical until the advent of songbirds, doves and the buzzing of aculeate wasps, and tail-cracking sounds by tinamous in the Cenozoic. The immense corpses of diplodocid sauropods appeared in the Upper Jurassic. sauropods were surrounded with the buzzing of legions of In the Lower Cretaceous, geckoes and birds joined the bottle flies, but not until the Upper Cretaceous. twilight chorus. The tapping of death-watch beetles and Historical Biology 281

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